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PROTOZOOLOGY

PROTOZOOLOGY
By

RICHARD

R.

KUDO,

D.Sc.

Professor of Zoology

The University
Urbana,

of Illinois

Illinois

With three hundred and seventy-six

illustrations

Fourth Edition

CHARLES

THOMAS

PUBLISHER
U.S.A.

Springfield, Illinois

Publisher Charles C Thomas Bannerstone House

301-327 East

Lawrence Avenue, Springfield, Illinois

Published simultaneously in the British Commonwealth oj Nations by Blackwell Scientific Publications, Ltd., Oxford, England

Published simultaneously in Canada by The Ryerson Press. Toronto

This monograph
part of
it

is

protected by copyright.

No

may

be reproduced in any manner

without written permission from the publisher.

Copyright 1931, 1939, 1946, and 1954 by Charles

C Thomas

Publisher

First Edition, January, 1931

Second Edition, September, 1939

Third Edition, January, 1946 Third Edition, Second Printing, November, 1947 Third Edition, Third Printing, August, 1950

Fourth Edition, September, 1954

Library of Congress Catalog Card

Number:

54-6567

Printed in the United States oj America

"The revelations

of the Microscope are perhaps not

excelled in importance

by those of the

telescope.

While exciting our curiosity, our wonder

and admiration, they have proved

infinite

of

service in advancing our

knowledge of things

around us."
Leidy

LIBRfcfcYl^

/^'
Preface

THE

fourth edition of Protozoology maintains

its

original

aim

in

setting forth "introductory information on the

common and

rep-

all groups of both free-living and parasitic Protozoa" for seniors and graduates in zoology in colleges and universities. It has been noted in recent years that students frequently wished to obtain a fuller knowledge on certain topics, organisms, processes, etc., than that which was found in the former edition. In order to meet this need without too great an expansion, references have been given to various items in the text and a list of a much larger number of literature has been appended to each chapter. Furthermore, this enlargement of references increases the usefulness of this work to advanced students, teachers of biology, field workers

resentative genera of

in various areas of biological science, veterinarians, physicians,

lic

pub-

health workers, laboratory diagnosticians and technicians, etc. While the chapter arrangement remains the same as before, a
in the

thorough revision has been carried on throughout the text

light

of

many

recently published contributions to protozoology.

Good

illustrations are indispensable in this kind of

work, since they

comprehended than lengthy statements. Therefore, old illustrations were replaced by more suitable ones and many new illustrations have been added, bringing up the total number of the text figures now to 376. Except diagrams, all figures are accompanied by the scales of magnification. For illustrations that have been adopted from published papers, the indebtedness of the author is expressed by mentioning the authors' names.
are far
easily

more

R. R.
Urbana, Illinois

Kudo

Contents
Preface Part I: General biology
CHAPTER
1

vii

Introduction
Relationship of protozoology to other fields of biological science, p. 6; the history of protozoology, p. 10.

Ecology
Free-living
zoa, p. 28.

20
Protozoa,
p.

20;

parasitic

Proto-

Morphology

39

The

nucleus, p. 40; the cytoplasm, p. 45; locomotor organellae, p. 49; fibrillar structures, p.
hold-fast
ratus,

60; protective or supportive organellae, p. 70; organellae, p. 76; parabasal appap. 77; Golgi apparatus, p. 78; chondriosomes, p. 80; contractile and other vacuoles, p.

83; chromatophore
p. 89.

and associated organellae,

97
112;

Physiology
Nutrition, p. 97; reserve food matter, p.
respiration, p. 116; excretion

and

secretion, p.

movements, Reproduction
118;

p. 122; irritability, p. 130.

145

Nuclear division, p. 145; cytoplasmic division, p. 166; colony formation, p. 173; asexual reproduction, p. 175; sexual reproduction and lifecycles, p. 180; regeneration, p. 212.

Variation and heredity

223

Part II: Taxonomy and special biology CHAPTER 7 Major groups and phylogeny of Protozoa Phylum Protozoa 8 Subphylum 1 Plasmodroma
Class

247

Subclass

Mastigophora 1 Phytomastigina Order 1 Chrysomonadina

1

249 254 254 254 256 256

IX

V "C30

CONTENTS
9
10
11

12
13

Order Order Order Order Order

2 Cryptomonadina
3
5

Phytomonadina
Chloromonadina

272 276
293 306 310

4 Euglenoidina 6 Dinoaagellata

Subclass 2 Zoomastigina

14
15
16
J

18 19

20
21

22
23 24

Order 1 Rhizomastigina Order 2 Protomonadina Order 3 Polymastigina Order 4 Hypermastigina Class 2 Sarcodina Subclass 1 Rhizopoda Order 1 Proteomyxa Order 2 Mycetozoa Order 3 Amoebina Order 4 Testacea Order 5 Foraminifera Subclass 2 Actinopoda Order 1 Heliozoa Order 2 Radiolaria Class 3 Sporozoa
Subclass
1

333 333 339 369 404 417 418 418 427 435 472 493 505 505 516 526 526 527 570 599 635 635 638 643 643

Telosporidia

25 26
27

Order 1 Gregarinida Order 2 Coccidia Order 3 Haemosporidia

Subclass 2 AcnidQsporidia

Order 1 Haplosporidia Order 2 Sarcosporidia

28
Subclass 3 Cnidosporidia

29

30

Order 1 Myxosporidia Order 2 Actinorayxidia Order 3 Microsporidia Order 4 Helicosporidia Subphylum 2 Ciliophora
Class
1

Ciliata
1

Subclass
31

Protociliata

Subclass 2 Euciliata

32
33

Order 1 Holotricha Suborder 1 Astomata Suborder 2 Gymnostomata Tribe 1 Prostomata Tribe 2 Pleurostomata

660 668 678 683 683 685 690 690 691 700 700 723

CONTENTS
34 35 36 37 38
39 40
41

xi

42 43 44 45

Tribe 3 Hypostomata Suborder 3 Trichostomata Suborder 4 Hymenostomata Suborder 5 Thigmotricha Suborder 6 Apostomea Order 2 Spirotricha Suborder 1 Heterotricha Suborder 2 Oligotricha Suborder 3 Ctenostomata Suborder 4 Hypotricha Order 3 Chonotricha Order 4 Peritricha
Class Suctoria
Collection, cultivation,

728 737 758 774 789 796

796 814 829 832 847 850 863 879 905 919

and observation

of

Protozoa

Author index
Subject index

PROTOZOOLOGY

PART

PROTOZOOLOGY I: GENERAL BIOLOGY

Chapter

Introduction

The body of a protozoan and manifests all characteristics common to the living thing. The various activities which make up the phenomena of life are carried on by parts within the body or cell. These parts are comparable with the organs of a metazoan which are composed of a large number of cells grouped into tissues and are called organellae or cell-organs. Thus the one-celled protozoan is a complete organism somewhat unlike the cell of a metazoan, each of which is dependent upon other cells and cannot live independently.
are unicellular animals.
cell
is

PROTOZOA

morphologically a single

From

this viewpoint, certain students of protozoology

maintain

that the Protozoa are non-cellular, and not unicellular, organisms.

Dobell (1911), for example, pointed out that the term "cell" is employed to designate (1) the whole protozoan body, (2) a part of a metazoan organism, and (3) a potential whole organism (a fertilized egg) which consequently resulted in a confused state of knowledge
regarding living things, and, therefore, proposed to define a cell as a mass of protoplasm composing part of an organism, and further
considered that the protozoan
ism, differently organized as
is

a non-cellular but complete organ-

compared with cellular organisms, the Metazoa and Metaphyta. Although some writers (Hyman, 1940;
Lwoff, 1951) follow this view, the great majority of protozoologists continue to consider the Protozoa as unicellular animals. Through the processes of organic evolution, they have undergone cytological
differentiation

and the Metazoa

histological differentiation.

In being unicellular, the Protozoa and the Protophyta are alike. The majority of Protozoa may be distinguished from the majority of

Protophyta on the basis

material,
all
it is

of dimensions,

methods

of nutrition, direc-

tion of division-plane, etc. While

not easy to detect

many Protophyta it in many forms; on

possess nuclear

the other hand,

binary

Protozoa contain at least one easily observable nucleus. The fission of Protozoa and Protophyta is longitudinal and transverse respectively. Most of Ciliata, however, multiply by transverse division. In general the nutrition of Protozoa is holozoic and of Protophyta, holophytic or saprophytic; but there are large numbers of Protozoa which nourish themselves by the latter methods. Thus an absolute and clean-cut separation of the two groups of unicellular
organisms
is

not possible. Haeckel (1866) coined the

name
is

Protista

to include these organisms in a single group, but this

not generally

PROTOZOOLOGY
it

adopted, since
ing an equal

includes undoubted animals and plants, thus creatof confusion

amount

between

it

plant. Calkins (1933) excluded chromatophore-bearing

and the animal or the Mastigoph-

ora from his treatment of Protozoa, thus placing organisms similar

every way, except the presence or absence of chromatophores, in different (animal and plant) groups. This intermingling of characteristics between the two groups of microorganisms shows clearly
in

two

their close interrelationship

and suggests strongly

their

common

ancestry.

Although the majority of Protozoa are solitary and the body is composed of a single cell, there are several forms in which the organism is made up of more than one cell. These forms, which are called colonial Protozoa (p. 173), are well represented by the members of Phytomastigina, in which the individuals are either joined by cytoplasmic threads or embedded in a common matrix. These cells are alike both in structure and in function, although in a few
be a differentiation of the individuals into reprocells. Unlike the cells in a metazoan which form tissues, these vegetative cells of colonial Protozoa are not so dependent upon other cells as are the cells in Metazoa; therefore, they do not form any true tissue. The reproductive cells produce zygotes through sexual fusion, which subsequently undergo repeated division and may produce a stage comparable with the blastula stage of a metazoan, but never reaching the gastrula stage. Thus, colonial Protozoa are only cell-aggregates without histological differentiation and may thus be distinguished from the Metazoa. An enormous number of species of Protozoa are known to man. From comparatively simple forms such as Amoeba, up to highly complicated organisms as represented by numerous ciliates, the Protozoa vary exceedingly in their body organization, morphological characteristics, behavior, habitat, etc., which necessitates a taxonomic arrangement for proper consideration as set forth in detail in Chapters 8 to 44.
ductive and vegetative
Relationship of protozoology to other fields of
biological science

forms there

may

brief

consideration of the relationship of Protozoology to

its

other fields of biology and

possible applications

may

not be

out of place here. Since the Protozoa are single-celled animals manifesting the characteristics common to all living things, they

have been studied by numerous investigators with a view to discovering the nature and mechanism of various phenomena, the

INTRODUCTION
sum-total of which

is known collectively as life. Though the investigators generally have been disappointed in the results, in-

asmuch

assumed simplicity of unicellular organisms has by the complexity of their cell-structure, nevertheless discussion of any biological principles today must take into account the information obtained from studies of Protozoa. It is now commonly recognized that adequate information on various types
as the

proved to be

offset

of

Protozoa

is

a prerequisite to a thorough comprehension of biology

of biological principles.
all

and to proper application

Practically

students agree in assuming that the higher types of animals have been derived from organisms which existed in the re-

mote past and which probably were somewhat

tive Protozoa of the present day. Since there
is

similar to the primi-

no sharp distinction between the Protozoa and the Protophyta or between the Protozoa and the Metazoa, and since there are intermediate forms between the major classes of the Protozoa themselves, progress in protozoology contributes toward the advancement of our knowledge on the probable steps by which living things in general evolved. Geneticists have undertaken studies on heredity and variation among Protozoa. "Unicellular animals," wrote Jennings (1909), "present all the problems of heredity and variation in miniature. The struggle for existence in a fauna of untold thousands showing as much variety of form and function as any higher group, works itself out, with ultimate survival of the fittest, in a few days under our eyes, in a finger bowl. For studying heredity and variation we get a generation a day, and we may keep unlimited numbers of pedigreed stock in a watch glass that can be placed under the microscope." Morphological and physiological variations are encountered commonly in all forms. Whether variation is due to germinal or environmental conditions, is often difficult to determine. Studies on conjugation in Paramecium by utilizing the mating types first noted by Sonneborn (1937, 1938) not only brought to light a wealth of important information regarding the genetics of Protozoa, but also are revealing a close insight concerning the relationship between the nuclear and cytoplasmic factors of heredity in the animal. Parasitic Protozoa are confined to one or more specific hosts. Through studies of the forms belonging to one and the same genus

among the host animals may The mosquitoes belonging to the genera Culex and Anopheles, for instance, are known to transmit avian and human Plasmodium respectively. They are further infected by
or species, the phylogenetic relation

be established or verified.

specific microsporidian parasites.

For instance, Thelohania

legeri

PROTOZOOLOGY

has been found widely only in many species of anopheline mosquitoes; T. opacita has, on the other hand, been found exclusively in culicine mosquitoes, although the larvae of the species belonging to these two genera live frequently in the same body of water (Kudo,

By observing certain intestinal Protozoa in some monHegner (1928) obtained evidence on the probable phylogenetic relationship between them and other higher mammals. The relation of various Protozoa of the wood-roach to those of the termite, as revealed by Cleveland and his associates (1934), gives further proof that the Blattidae and the Isoptera are closely related. Study of a particular group of parasitic Protozoa and their hosts may throw light on the geographic condition of the earth which existed in the remote past. The members of the genus Zelleriella are usually found in the colon of the frogs belonging to the family Leptodactylidae. Through an extensive study of these amphibians from South America and Australia, Metcalf (1920, 1929) found that the species of Zelleriella occurring in the frogs of the two continents are almost identical. He finds it more difficult to conceive of convergent or parallel evolution of both the hosts and the parasites, than to assume that there once existed between Patagonia and Australia a land connection over which frogs, containing Zelleriella, migrated. Experimental studies of large Protozoa have thrown light on the relation between the nucleus and the cytoplasm, and have furnished a basis for an understanding of regeneration in animals. In Protozoa we find various types of nuclear divisions ranging from a simple amitotic division to a complex process comparable in every detail with the typical metazoan mitosis. A part of our knowledge in cytology is based upon studies of Protozoa. Through the efforts of various investigators in the past fifty years, it has now become known that some 25 species of Protozoa occur in man. Entamoeba histolytica, Balantidium coli, and four species of Plasmodium, all of which are pathogenic to man, are
1924, 1925).

keys,

widely distributed throughout the world. In certain restricted areas are found other pathogenic forms, such as Trypanosoma and Leishmania. Since all parasitic Protozoa presumably have originated in free-living forms and since our knowledge of the morphology, physiology, and reproduction of the parasitic forms has largely been obtained in conjunction with the studies of the free-living organisms, a general

knowledge

of the entire

phylum

is

necessary to under-

stand these parasitic forms.

Recent studies have further revealed that almost all domestic animals are hosts to numerous parasitic Protozoa, many of which

INTRODUCTION
are responsible for serious infectious diseases.

Some

of

the forms

found in domestic animals are morphologically indistinguishable from those occurring in man. Balantidium coli is considered as a parasite of swine, and man is its secondary host. Knowledge of protozoan parasites is useful to medical practitioners, just as it is essential to veterinarians inasmuch as certain diseases of animals, such as southern cattle fever, dourine, nagana, blackhead, coccidiosis, etc., are caused by Protozoa. Sanitary betterment and improvement are fundamental requirements in the modern civilized world. One of man's necessities is safe drinking water. The majority of Protozoa live freely in various bodies of water and some of them are responsible, if present in sufficiently large numbers, for giving certain odors to the waters of reservoirs or ponds (p. 114). But these Protozoa which are occasionally harmful are relatively small in number compared with those which are beneficial to man. It is generally understood that bacteria live on various waste materials present in the polluted water, but that upon reaching a certain population, they would cease to multiply and would allow the excess organic substances to undergo decomposition. Numerous holozoic Protozoa, however, feed on the bacteria and prevent them from reaching the saturation population. Protozoa thus seem to help indirectly in the purification of the water. Protozoology therefore must be considered as part of modern sanitary science.

Young

fish

feed extensively on small aquatic organisms, such as

all of which depend largely upon Protozoa and Protophyta as sources of food supply. Thus the fish are indirectly dependent upon Protozoa as food material. On the other hand, there are numbers of Protozoa which live at the expense of fish. The Myxosporidia are almost exclusively parasites of fish and sometimes cause death to large numbers of commercially important fishes (Kudo, 1920) (p. 648). Success in fish-

larvae of insects, small crustaceans, annelids, etc.,

culture, therefore, requires

among

other things a thorough knowl-

edge of Protozoa. Since Russel and Hutchinson (1909) suggested some forty years ago that Protozoa are probably a cause of limitation of the numbers, and therefore the activities of bacteria in the soil and thus tend to
decrease the

amount

of nitrogen

which

is

given to the

soil

by the

nitrifying bacteria, several investigators

have brought out the fact

that in the soils of temperate climate various sarcodinans, flagellates and less frequently ciliates, are present and active throughout the
year.

The exact

relation

between

specific

Protozoa and bacteria

in

10

PROTOZOOLOGY
soil is

the

not yet clear in spite of the numerous experiments and

observations. All soil investigators should be acquainted with the

biology and
It is

taxonomy

of free-living Protozoa.

honey bee
in

that the silkworm and the from microsporidian infections (p. 670). Sericulture south-western Europe suffered great damages in the middle of
suffer

a matter of

common knowledge

the nineteenth century because of the "pebrine" disease, caused by

the microsporidian,

Nosema

bombycis. During the

first

decade
apis,

of

the present century, another microsporidian,

found to infect a large number of honey bees. of control have been developed and put into practice so that these microsporidian infections are at present not serious, even though they still occur. On the other hand, other Microsporidia are now known to infect certain insects, such as mosquitoes and lepidopterous pests,
which,

Nosema Methods

was

when heavily

infected, die sooner or later.

struction of these insects

by means

of chemicals are

used, but attention should also be given to

Methods of demore and more biological control of them

of Protozoa and Protophyta. While the majority of Protozoa lack permanent skeletal structures and their fossil forms are little known, there are at least two large groups in the Sarcodina which possess conspicuous shells and which are found as fossils. They are Foraminifera and Radiolaria. From

by means

early palaeozoic era

down

to the present day, the carbonate of

lime which makes

been

left

up the skeletons of numerous Foraminifera has embedded in various rock strata. Although there is no dis-

tinctive foraminiferan fauna characteristic of a given geologic pe-

Foraminifera which disthis fact one can understand that knowledge of foraminiferous rocks is highly useful in checking up logs in well drilling. The skeletons of the Radiolaria are
riod, there are certain peculiarities of fossil

tinguish one formation from the other.

From

the main constituent of the ooze of littoral and deep-sea regions.

They have been found abundantly in siliceous rocks of the palaeozoic and the mesozoic eras, and are also identified with the clays and other formations of the miocene period. Thus knowledge of these two
orders of Sarcodina, at least,
is

essential for the student of geology

and paleontology.

The

history of protozoology

Aside from a comparatively small number of large forms, Protozoa are unobservable with the naked eye, so that one can easily understand why they were unknown prior to the invention of the microscope.

Antony van Leeuwenhoek (1632-1723)

is

commonly

recog-

INTRODUCTION
nized
as

11

the

father

of

protozoology.

Grinding lenses

himself,

Leeuwenhoek made more than 400 simple lenses, including one which, it is said, had a magnification of 270 times (Harting). Among
the

many

things he discovered were various Protozoa. According

Leeuwenhoek saw in 1674 for the first time freeBetween 1674 and 1716, he observed many Protozoa which he reported to the Royal Society of London and which, as Dobell interpreted, were Euglena ("green in the middle, and before and behind white"), Vorticella, Stylonychia,
to Dobell (1932),
living fresh- water Protozoa.

Carchesium, Volvox, Coleps, Kerona, Anthophysis, Elphidium, etc. Huygens gave in 1678 "unmistakable descriptions of Chilodon(-ella), Paramecium, Astasia and Vorticella, all found in infusions" (Dobell).

Colpoda was seen by Buonanni (1691) and Harris (1696) rediscovered Euglena. In 1718 there appeared the first treatise on microscopic organisms, particularly of Protozoa,
sized the non-existence of abiogenesis
in

by Joblot who emphaby using boiled hay-infusions

which no Infusoria developed without exposure to the atmosphere. This experiment confirmed that of Redi who, some 40 years before, had made his well-known experiments by excluding flies from meat. Joblot illustrated, according to Woodruff (1937), Paramecium,
the slipper animalcule, with the
(1744) studied division in
first identifiable figure. Trembley some ciliates, including probably Paramecium, which generic name was coined by Hill in 1752. Noctiluca was first described by Baker (1753). Rosel von Rosenhof (1755) observed an organism, which he called "der kleine Proteus," and also Vorticella, Stentor, and Volvox. The "Proteus" which Linnaeus named Volvox chaos (1758) and later renamed Chaos protheus (1767), cannot be identified with any of the known amoeboid organisms (Kudo, 1946). Wrisberg (1764) coined

the term "Infusoria" (Dujardin; Woodruff).

By

using the juice of

caused the extrusion of the "fins" (trichocysts) in Paramecium. Eichhorn (1783) observed the heliozoan, Actinosphaerium, which now bears his name. O. F. Miiller described
geranium,
Ellis (1769)

and published two works on the Infusoria some Metazoa and Protophyta in his monographs, some of his descriptions and figures of Ciliata were so well done that they are of value even at the present
Ceratium a
little later

(1773, 1786) although he included unavoidably

time.

Lamarck (1816) named Folliculina. At the beginning of the nineteenth century the cylcosis in Paramecium was brought to light by Gruithuisen. Goldfuss (1817) coined the term Protozoa, including in it the coelenterates. Nine years
later there

appeared d'Orbigny's systematic study of the Foramini-

12
fera,

PROTOZOOLOGY

which he considered "microscopical cephalopods." In 1828 Ehrenberg began publishing his observations on Protozoa and in 1838 he summarized his contributions in Die Infusionsthicrchen als vollkommene Organismen, in which he diagnosed genera and species so well that many of them still hold good. Ehrenberg excluded Rotatoria and Cercaria from Infusoria. Through the studies of Ehrenberg the number of known Protozoa increased greatly; he, however, proposed the term "Polygastricha," under which he placed Mastigophora, Rhizopoda, Ciliata, Suctoria, desmids, etc., since he believed that the food vacuoles present in them were stomachs. This hypothesis became immediately the center of controversy, which incidentally, together with the then-propounded cell theory and improvements in microscopy, stimulated researches on Protozoa. Dujardin (1835) took pains in studying the protoplasm of various Protozoa and found it alike in all. He named it sarcode. In 1841 he published an extensive monograph of various Protozoa which came under his observations. The term Rhizopoda was coined by this investigator. The commonly used term protoplasm was employed by Purkinje (1840) in the same sense as it is used today. The Protozoa was given a distinct definition by Siebold in 1845, as follows: "Die Thiere, in welchen die verschiedenen Systeme der Organe nicht
scharf ausgeschieden sind,

und deren unregelmassige Form und

ein-

fache Organization sich auf eine Zelle reduzieren lassen." Siebold

entiation of Protozoa as a group certainly inspired

subdivided Protozoa into Infusoria and Rhizopoda. The sharp differnumerous micros-

copists. As a result, several students brought forward various group names, such as Radiolaria (J. Muller, 1858), Ciliata (Perty, 1852), Flagellata (Cohn, 1853), Suctoria (Claparede and Lachmann, 1858), Heliozoa, Protista (Haeckel, 1862, 1866), Mastigophora (Diesing, 1865), etc. Of Suctoria, Stein failed to see the real nature (1849), but his two monographs on Ciliata and Mastigophora (1854, 1859-1883)

contain concise descriptions and excellent illustrations of numerous

species.

Haeckel who went a step further than Siebold by distinguish-

ing between Protozoa and Metazoa, devoted 10 years to his study

scribed in his celebrated

Challenger collection, and demonographs more than 4000 species. In 1879 the first comprehensive monograph on the Protozoa of North America was put forward by Leidy under the title of Freshwater Rhizopods of North America, which showed the wide distribution of many known forms of Europe and revealed a number of new and interesting forms. This work was followed by Stokes' The Freshwater Infusoria of the United States, which appeared in 1888.
of Radiolaria, especially those of the

INTRODUCTION
Butschli (1880-1889) established Sarcodina and
contribution to the

13

made an excellent then-known species of Protozoa, which is still considered as one of the most important works on general protozoology. The painstaking researches by Maupas, on the
taxonomy
of the

conjugation of

ciliates,

corrected erroneous interpretation of the

phenomenon observed by Balbiani some 30 years before and gave impetus to a renewed cytological study of Protozoa. The variety in form and structure of the protozoan nuclei became the subject of intensive studies by several cytologists. Weismann put into words the
immortality of the Protozoa. Schaudinn contributed much toward the cytological and developmental studies of Protozoa. In the first year of the present century, Calkins in the United States and Dofiein in Germany wrote modern textbooks of protozoology dealing with the biology as well as the taxonomy. Jennings devoted his time for nearly 40 years to the study of genetics of Protozoa. Recent development of bacteria-free culture technique in certain flagellates

and

ciliates,

has brought to light important informa-

tion regarding the nutritional requirements

and metabolism

of these

organisms.
sively studied

are more and more intensively and extenfrom both the biological and the parasitological sides, and important contributions appear continuously. Since all parasitic Protozoa appear to have originated in free-living forms, the comprehension of the morphology, physiology, and development of the latter group is obviously fundamentally important for a thorough

Today the Protozoa

understanding of the former group. Compared with the advancement of our knowledge on free-living Protozoa, that on parasitic forms has been very slow. This is to be expected, of course, since the vast majority of them are so minute that the discovery of their presence has been made possible only through improvements in the microscope and in technique. Here again Leeuwenhoek seems to have been the first to observe
the a parasitic protozoan, for he observed, according to Dobell (1932), in fall of 1674, the oocysts of the coccidian Eimeria stiedae, in the

contents of the gall bladder of an old rabbit; in 1681, Giardia intestinalis in his

own

diarrhceic stools;

and

in 1683,

Opalina and Nyctoof

therus in the gut contents of frogs.

The

oral

Trichomonas

man was

observed by O. F. Miiller (1773) who named it Cercaria tenax (Dobell, 1939). There is no record of anyone having seen Protozoa living in other organisms, until 1828, when Dufour's account of the gregarine from the intestine of coleopterous insects appeared. Some ten
years later,

Hake

rediscovered the oocysts of Eimeria stiedae.

14

PROTOZOOLOGY

flagellate was observed in the blood of salmon by Valentin in 1841, and the frog trypanosome was discovered by Gluge (1842) and

Gruby
for
it.

(1843), the latter author creating the genus

Trypanosoma

little later given attention by Kolliker The year 1849 marks the first record of an amoeba being found in man, for Gros then observed Entamoeba

The

gregarines were a
(1848).

(1848)

and Stein

gingivalis in the

human mouth.

Five years

later,

in the stools of cholera patients

two

flagellates

Davaine found (Trichomonas and

cina, in the excretory

Chilomastix). Kloss in 1855 observed the coccidian, Klossia heliorgan of Helix; and Eimer (1870) made an ex-

tensive study of Coccidia occurring in various animals. Balantidium

coli

was discovered by Malmsten in 1857. Lewis in 1870 observed Entamoeba coli in India, and Losch in 1875 found Entamoeba histolytica in Russia. During the early part of the last century, an epidemic disease, pebrine, of the silkworm appeared in Italy and France, and a number of biologists became engaged in its investigation. Foremost of all, Pasteur (1870) made an extensive report on the nature of the causative organism, now known as Nosema bombycis, and also on the method of control and prevention. Perhaps this is the first scientific study of a parasitic protozoan which resulted in an effective
practical

method

of control of its infection.

in 1878 an organism which is since known as Trypanosoma lewisi in the blood of rats. In 1879 Leuckart created the group Sporozoa, including in it the gregarines and coccidians. Other groups under Sporozoa were soon definitely designated. They are Myxosporidia (Butschli, 1881), Microsporidia and Sarcosporidia

Lewis observed

(Balbiani, 1882).
Parasitic

protozoology received a far-reaching stimulus when

Laveran (November, 1880) discovered the microgamete formation ("flagellation") of a malaria parasite in the human blood. Smith and Kilborne (1893) demonstrated that Babesia of the Texas fever of cattle in the southern United States was transmitted by the cattle tick from host to host, and thus revealed for the first time the close relationship which exists between an arthropod and a parasitic protozoan. Two years later Bruce discovered Trypanosoma brucei in the blood of domestic animals suffering from "nagana" disease in Africa and later (1897) demonstrated by experiments that the tsetse fly transmits the trypanosome. Studies of malaria organisms continued and several important contributions appeared. Golgi (1886, 1889) studied the schizogony and its relation to the occurrence of fever, and was able to distinguish the types of fever. MacCallum (1897)

INTRODUCTION

15

observed the microgamete formation in Haemoproteus of birds and suggested that the "flagella" observed by Laveran were microgametes of Plasmodium. In fact, he later observed the formation of
the zygote through fusion of a microgamete and a macrogamete of Plasmodium falciparum. Almost at the same time, Schaudinn and
Siedlecki (1897)

showed that anisogamy

results in the production of

zygotes in Coccidia.

The

latter author published later further ob-

servations on the life-cycle of Coccidia (1898, 1899).

r dictum

Ross (1898, 1898a) revealed the development of Plasmodium (P. praecox) in Culex fatigans and established the fact that the host birds become infected by this protozoan through the bites of the infected mosquitoes. Since that time, investigators too numerous to mention here (p. 600), studied the biology and development
of the malarial organisms. Among the more recent findings is the exo-erythrocytic development, fuller information on which is now being sought. In 1902, Dutton found that the sleeping sickness in

equatorial Africa
biense.

was caused by an infection by Trypanosoma gamIn 1903, Leishman and Donovan discovered simultaneously Leishmania donovani, the causative organism of "kala-azar" in
Artificial cultivation of bacteria

India.

rapid advancement in bacteriology, and

had contributed toward a very it was natural, as the num-

ber of

cultivate

known parasitic Protozoa rapidly increased, that attempts to them in vitro should be made. Musgrave and Clegg (1904)
amoebae from
old

cultivated, on bouillon-agar, small free-living

faecal matter. In 1905

Novy and MacNeal cultivated

successfully the

trypanosome of birds in blood-agar medium, which remained free from bacterial contamination and in which the organisms underwent multiplication. Almost all species of Trypanosoma and Leishmania have since been cultivated in a similar manner. This serves for detection of a mild infection and also identification of the species involved. It was found, further, that the changes which these organisms underwent in the culture media were imitative of those that took place in the invertebrate host, thus contributing toward the
life-cycle studies of

them.

During and since World

War

I, it

became known that numer-

ous intestinal Protozoa of man are widely present throughout the tropical, subtropical and temperate zones. Taxonomic, morphological and developmental studies on these forms have therefore ap-

peared

in an enormous number. Cutler (1918) seems to have succeeded in cultivating Entamoeba histolytica, though his experiment was not repeated by others. Barret and Yarborough (1921) culti-

1G

PROTOZOOLOGY

vated Balantidium
mesnili.

coli and Boeck (1921) cultivated Chilomastix Boeck and Drbohlav (1925) succeeded in cultivating Entamoeba histolytica, and their work was repeated and improved upon by many investigators. While the in-vitro cultivation has not thrown much light on metabolic activities of this and other parasitic amoebae, as no one of them would grow in culture without some other organisms, it has increased our knowledge on the biology of

these parasites.

References

Allman, G.
177.

the occurrence among the Infusoria of peculiar organs resembling thread-cells. Quart J. Micr. Sc., 3:
J.:

(1855)

On

Baker, H.: (1753) Employment

for the microscope. London. Balbiani, G.: (1882) Sur les microsporidies ou psorospermies des articules. C. R. Acad. Sc, 95:1168. Barret, H. P. and Yarbrough, N. (1921) A method for the cultivation of Balantidium coli. Am. J. Trop. Med., 1:161. Boeck, W. C. (1921) Chilomastix mesnili and a method for its culture. J. Exper. Med., 33:147. -and Drbohlav, J.: (1925) The cultivation of Endamoeba histolytica. Am. J. Hyg., 5:371. Bruce, D. (1895) Preliminary report on the tsetse fly disease or
: : :

in Zululand. Umbobo. (1897) Further report, etc. Umbobo. Butschli, 0.: (1880-1889) Protozoa. Bronn's Klassen und Ordnungen des Thierreichs. Vols. 1-3. (1881) Myxosporidia. Zool. Jahrb. 1880, 1 162. Buonanni, F.: (1691) Observationes circa Viventia, etc. Rome. Calkins, G. N.: (1901) The Protozoa. Philadelphia. (1933) The biology of the Protozoa. 2 ed. Philadelphia. Claparede, J. L. R. A. E. and Lachmann, J.: (1858-59) Etudes sur les Infusoires et les Rhizopodes. Vol. 1. Geneva. Cleveland, L. R., Hall, S. R. and Sanders, E. P.: (1934) The woodfeeding roach, Cryptocercus, its Protozoa, and the symbiosis between Protozoa and roach. Mem. Am. Acad. Arts & Sc, 17:185. Cohn, F. J.: (1853) Beitrage zur Entwickelungsgeschichte der Infusorien. Zeitschr. wiss. Zool., 6:253. Cole, F. J.: (1926) The history of protozoology. London. Cutler, D. W. (1918) method for the cultivation of Entamoeba histolytica. J. Path. Bact., 22:22. Davaine, C. (1854) Sur des animalcules infusoires, etc. C. R. Soc Biol., 1:129. Dobell, C: (1911) The principles of protistology. Arch. Protist.,

nagana

23:269. (1932)

Antony van Leeuwenhoek and

his "little animals."

New

York.

(1939)

The common

flagellate of the

human mouth,

Tri-

INTRODUCTION
chomonas tenax (O.F.M.)
Parasit., 31:138.
: :

17
its

its

discovery and
als Parasiten

nomenclature.

Doflein, F. (1901) Die Protozoen

reger. Jena.

und Krankheitser-

and Reichenow,
5 ed. Jena. Donovan, C. (1903)
:

E.: (1929)
of

Lehrbuch der Protozoenkunde.

one of the heterogeneous fevers
la Classe des

in India. Brit.
:

The etiology M. J., 2:1401.

d'Orbigny, A. (1826) Tableau methodique de opodes. Ann. Sci. Nat., 7:245.

Cephal-

Dufour,

Dujardin,

L.: (1828) Note sur la gregarine, etc. Ibid., 13:366. F. (1835) Sur les pretendus estomacs des animalcules
:

infusoires et sur
Zool., 4:343.

une substance appelee sarcode. Ann.

Sci.

Nat.

(1841) Histoire naturelle des zoophytes. Infusoires. Paris. J. E. (1902) Preliminary note upon a trypanosome occurring in the blood of man. Rep. Thomson Yates Lab., 4:455. Ehrenberg, C. G.: (1838) Die Infusionsthierchen als vollkommene Organismen. Leipzig. Eichhorn, J. C: (1783) Zugabe zu meinen Beytragen, etc. Danzig. Eimer, T. (1870) Ueber die ei- und kugelformigen sogenannten Psorospermien der Wirbelthiere. Wurzburg. Ellis, J.: (1769) Observations on a particular manner of increase in the animalcula, etc. Phil. Trans., 59:138. Gluge, G. (1842) Ueber ein eigenthumliches Entozoon im Blute des Frosches. Arch. Anat. Phys. wiss. Med., 148. Goldfuss, G. A.: (1817) Ueber die Entwicklungsstufen des Thieres.

Dutton,

Nurnberg. Golgi, C.: (1886) Sulla infezione malarica. Arch.

Sci. Med., 10:109. (1889) Sul ciclo evolutio dei parassiti malarici nella febbre terzana, etc. Ibid., 13:173. Gros, G.: (1849) Fragments d'helminthologie et de physiologie microscopique. Bull. Soc. Imp. Nat. Moscou, 22:549. Gruby, D.: (1843) Recherches et observations sur une nouvelle espece d'hematozoaire, Trypanosoma sanguinis. C. R. Acad. Sc,

17:1134.

Haeckel, E. H.:

(1862) Betrachtungen ueber die Grenzen und Verwandschaft der Radiolarien und ueber die Systematik der

Rhizopoden im Allgemeinen. Berlin. (1866) Generelle Morphologie der Organismen. Berlin. Hake, T. G.: (1839) A treatise on varicose capillaries, as constituting the structure of carcinoma of the hepatic ducts, etc. London.
J.: (1696) Some microscopical observations of vast numbers of animalcula seen in water. Phil. Trans., 19:254. Hegner, R. (1928) The evolutionary significance of the protozoan parasites of monkeys and man. Quart. Rev. Biol., 3:225. Hill, J. (1752) An history of animals, etc. London. Hyman, Libbie H. (1940) The invertebrates: Protozoa through

Harris,

Ctenophora.

New

York.

IS

PROTOZOOLOGY
S.
:

Jennings, H.
:

(1909) Heredity and variation in the simplest organisms. Am. Nat., 43:322. Joblot, L. (1718) Descriptions et usages de plusieurs nouveaux microscopes, etc. Paris. Kloss, H.: (1855) Ueber Parasiten in der Niere von Helix. Abh. Senckenb. Naturf. Ges., 1:189. Kolliker, A.: (1848) Beitrage zur Kenntnis niederer Thiere. Zeitschr. wiss. Zool., 1:34. Kudo, R. R. (1920) Studies on Myxosporidia. Illinois Biol. Monogr. 5:nos. 3, 4. (1924) Studies on Microsporidia parasitic in mosquitoes.
:

III.

Arch. Protist., 49:147.

(1925) IV. Centralbl. Bakt. I. Orig., 96:428. (1946) Pelomyxa carolinensis Wilson. I. Jour. Morph., 78: 317. Laveran, A.: (1880) Note sur un nouveau parasite trouve dans le sang de plusieurs malades atteints de fievre palustre. Bull Acad. Med., 9:1235, 1268, 1346. (1880a) Un nouveau parasite trouve dans le sang des malades atteints de fievre palustre. Bull. Mem. Soc. Med. Hopit. Paris, 17:158. Leidy, J.: (1879) Freshwater Rhizopods of North America. Rep. U. S. Geol. Survey, 12. Leishman, W. B.: (1903) On the possibility of the occurrence of trypanosomiasis in India. British Med. Jour., 1:1252. Leuckart, R. (1879) Die Parasiten des Menschen. 2 ed. Leipzig. Lewis, T. R. (1870) report on the microscopic objects found in cholera evacuations, etc. Ann. Rep. San. Comm. Gov. India (1869) 6:126. (1878) The microscopic organisms found in the blood of man and animals, etc. Ibid. (1877) 14:157. Linnaeus, C.: (1758) Systema Naturae. 10 ed. 1:820. (1767) Systema Naturae. 12 ed. 1:1324. Losch, F. (1875) Massenhafte Entwickelung von Amoben im Dickdarm. Arch. path. Anat., 65:196. Lwoff, A.: (1951) Biochemistry and physiology of Protozoa. New
:

York.

MacCallum, W.

G.: (1897) On the flagellated form of the malarial parasite. Lancet, 2:1240. Malmsten, P. H.: (1857) Infusorien als Intestinal-Thiere beim

Menschen. Arch. path. Anat., 12:302. Metcalf, M. M.: (1920) Upon an important method of studying problems of relationship and of geographical distribution. Proc.
Nat. Acad. Sc, 6:432.
(1929) Parasites

omy, geographical
Misc. Coll., 81: no.

and the aid they give in problems of taxondistribution, and paleogeography. Smith.
8.
:

Musgrave, W. E. and Clegg, M. T. (1904) Amebas: their cultivation and aetiologic significance. Dep. Inter., Biol. Lab. Bull.,
Manila, no. 18:1.

INTRODUCTION
Novy,
F. G.
:

19

and MacNeal, W.

J.:

(1905)

On

the trypanosomes of

birds. J. Inf. Dis., 2:256.

Pasteur, L. (1870) Etudes sur la maladie des vers a soie. Paris. Perty, M.: (1852) Zur Kenntnis kleinster Lebensformen, etc. Bern. Rosel von Rosenhof, A. J.: (1755) Der kleine Proteus. Der
Monat.-herausgeg. Insect. -Belust., 3:622. Ross, R.: (1898) Report on the cultivation of Proteosoma Labbe in grey mosquitoes. Gov. Print. Calcutta. (1898a) Preliminary report on the infection of birds with Proteosoma by the bites of mosquitoes. Ibid. Russell, E. J. and Hutchinson, H. B.: (1909) The effect of partial sterilization of soil on the production of plant food. J. Agr. Sc,
3:111.
F. and Siedlecki, M.: (1897) Beitrage zur Kenntnis der Coccidien. Verhandl. deut. zool. Ges., p. 192. Siebold, C. T. v.: (1845) Bericht ueber die Leistungen in der Naturgeschichte der Wiirmer, etc. Arch. Naturg., 11:256. Siedlecki, M.: (1898) Etude cytologique et cycle evolutif de la coccidie de la seiche. Ann. Inst. Pasteur, 12:799. Etude cytologique et cycle evolutif de Adelea ovata Schneider. Ibid., 13:169. Smith, T. and Kilborne, F. L. (1893) Investigations into the nature, causation, and prevention of Texas or southern cattle fever. Bull. Bur. Animal Ind., U. S. Dep. Agr., No. 1. Sonneborn, T. M. (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc. Nat. Acad. Sc, 23:378. (1938) Mating types in Paramecium aurelia, etc. Proc. Am. Phil. Soc, 79:411. Stein, S. F. N. v.: (1854) Die Infusionsthiere auf ihre Entwickelungsgeschichte untersucht. Leipzig. (1859-83) Der Organismus der Infusionsthiere. Leipzig. Stokes, A. C: (1888) A preliminary contribution toward a history of the fresh-water Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71. Trembley, A.: (1744) Observations upon several newly discovered species of freshwater polypi. Phil. Trans., 43:169. Valentin: (1841) Ueber ein Entozoon im Blute von Salmo fario. Arch. Anat. Phys. wiss. Med., p. 435. Woodruff, L. L. (1937) Louis Joblot and the Protozoa. Sc Monthly, 44:41. (1939) Some pioneers in microscopy, with special reference to protozoology. Tr. N. Y. Acad. Sc, Ser. 2, 1:74. Wrisberg, H. A.: (1765) Observationum de Animalculis infusoriis Satura. Gottingen.

Schaudinn,

Chapter

Ecology

WITH
tic.

regard to their habitats, the Protozoa

may

be divided

and those living on or in other organisms. Mastigophora, Sarcodina, Ciliata, and Suctoria include both freeliving and parasitic Protozoa, but Sporozoa are exclusively parasiinto free-living forms

Free-living Protozoa

The vegetative
found
in

or trophic stages of free-living Protozoa

soil

every type of fresh and salt water,

have been and decaying or-

in the circumpolar regions or at extremely high protozoa occur at times in fairly large numbers. The factors, which influence their distribution in a given body of water, are temperature, light, chemical composition, acidity, kind and amount of food, and degree of adaptability of the individual protozoans to various environmental changes. Their early appearance as

ganic matter.

Even

altitudes, certain

living organisms, their adaptability to various habitats,

and

their ca-

pacity to remain viable in the encysted condition, probably account for the wide distribution of the Protozoa throughout the world. The

common

free-living

mention a few,

of fresh waters,

amoebae, numerous testaceans and others, to have been observed in innumerable

of

places of the world.

Temperature. The majority

Protozoa are able to

live only

within a small range of temperature variation, although in the en-

cysted state they can withstand a far greater temperature fluctuais marked by the freezing of by the destructive chemical change within the body protoplasm. The temperature toleration seems to vary among different species of Protozoa; and even in the same species under different conditions. For example, Chalkley (1930) placed Paramecium caudatum in 4 culture media (balanced saline, saline with potassium excess, saline with calcium excess, and

tion.

The lower

limit of the temperature

the protoplasm, and the upper limit

sodium excess), all with pH from 5.8 or 6 to 8.4 or 8.6, at 40C. for 2-16 minutes and found that (1) the resistance varies with
saline with

the hydrogen-ion concentration,

maxima appearing

in the alkaline

and acid ranges, and a minimum at or near about 7.0; (2) in a balanced saline, and in saline with an excess of sodium or potassium, the alkaline maximum is the higher, while in saline with an excess of
calcium, the acid
creases

maximum

is

the higher; (3) in general, acidity de(4)

and alkalinity increases resistance; and

20

between

pH

6.6

ECOLOGY

21

and 7.6, excess of potassium decreases resistance and excess of calcium increases resistance. Glaser and Coria (1933) cultivated Paramecium caudatum on dead yeast free from living organisms at 20-28C. (optimum 25C.) and noted that at 30C. the organisms were killed. Doudoroff (1936), on the other hand, found that in P. multimicronucleatum its resistance to raised temperature was low in the presence of food, but rose to a maximum when the food was exhausted, and there was no appreciable difference in the resistance between single and conjugating individuals. The thermal waters of hot springs have been known to contain living organisms including Protozoa. Glaser and Coria' (1935) obtained from the thermal springs, of Virginia, several species of Mastigophora, Ciliata, and an amoeba which were living in the water, the temperature of which was 34-36C, but did not notice any protozoan in the water which showed 39-41C. Uyemura (1936, 1937) made a series of studies on Protozoa living in various thermal waters of Japan, and reported that many species lived at unexpectedly high temperatures. Some of the Protozoa observed and the temperatures of the water in which they were found are as follows: Amoeba sp., Vahlkampfia Umax, A. radiosa, 30-51C; Amoeba verrucosa, Chilodonella sp., Lionotus fasciola, Paramecium caudatum, 36-40C;
Oxytricha fallax, 30-56C.

Under experimental
the change be

conditions,

it

has been shown repeatedly that

to a very high temperature
if

many protozoans become accustomed

made

gradually. Dallinger (1887)

showed a long time

flagellates

ago that Tetramitus rostratus and two other species of

became gradually acclimatized up

ture,

to 70C. in several years. In na-

however, the thermal death point of most of the free-living Protozoa appears to lie between 36 and 40C. and the optimum temperature, between 16 and 25C. On the other hand, the low temperature seems to be less detrimental to Protozoa than the higher one. Many protozoans have been found to live in water under ice, and several haematochromebearing Phytomastigina undergo vigorous multiplication on snow in high altitudes, producing the so-called "red snow." Klebs (1893) subjected the trophozoites of Euglena to repeated freezing without apparent injury and Jahn (1933) found no harmful effect when Euglena cultures were kept without freezing at 0.2C. for one hour, but

when kept

at

4C.

for one

hour the majority were

killed.

Gay lord

(1908) exposed Trypanosoma gambiense to liquid air for 20 minutes

without apparent injury, but the organisms were killed after 40 minutes' immersion,

22

PROTOZOOLOGY

ill

Kiihne (1864) observed that Amoeba and Actinophrys suffered no effects when kept at 0C. for several hours as long as the culture medium did not freeze, but were killed when the latter froze. Molisch

(1897) likewise noticed that

its

Amoeba

dies as soon as the ice forms in

interior or

immediate

vicinity.

Chambers and Hale

(1932)

onstrated that internal freezing could be induced in an

inserting an ice-tipped pipette at

demamoeba by

0.6C,

the ice spreading in the

from the point touched by the pipette. They found that the internal freezing kills the amoebae, although if the ice is prevented from forming, a temperature as low as 5C. brings about no visible damage to the organism. At 0C, Deschiens (1934) found the trophozoites of Entamoeba histolytica remained alive, though immobile, for 56 hours, but were destroyed in a short
form
of fine featherly crystals

time when the

medium

froze at

5C.

According to Greeley (1902), when Stentor coeruleus was slowly subjected to low temperatures, the cilia kept on beating at 0C. for 1-3 hours, then cilia and gullet were absorbed, the ectoplasm was thrown off, and the body became spherical. When the temperature was raised, this spherical body is said to have undergone a reverse process and resumed its normal activity. If the lowering of temperature
is

rapid and the

medium becomes

solidly frozen, Stentor per-

ishes.

Efimoff (1924) observed that Paramecium multiplied once in about 13 days at 0C, withstood freezing at 1C. for 30 minutes

but died when kept for 50-60 minutes at the same temperature. He further stated that Paramecium caudatum, Colpidium colpoda, and Spirostomum ambiguum, perished in less than 30 minutes, when exposed below 4C, and that quick and short cooling (not lower than 9C.) produced no injury, but if it is prolonged, Paramecium became spherical and swollen to 4-5 times normal size, while Colpidium and Spirostomum shrunk. Wolfson (1935) studied Paramecium sp. in gradually descending subzero-temperature, and observed that as the temperature decreases the organism often swims backward, its bodily movements cease at 14.2C, but the cilia continue to beat for some time. While Paramecium recover completely from a momentary exposure to 16C, long cooling at this temperature brings about degeneration. When the water in which the organisms are kept freezes, no survival was noted. Plasmodium knowlcsi and P. inui in the blood of Macacus rhesus remain viable, according to Coggeshall (1939), for as long as 70 days at 76C, if frozen and hawed rapidly. Low temperature on Protozoa (Luyet and Gehenio,
1

1940).

Light. In the Phytomastigina

which include chromatophore-bear-

ECOLOGY

23

ing flagellates, the sun light is essential to photosynthesis (p. 107). The sun light further plays an important role in those protozoans which are dependent upon chromatophore-possessing organisms as chief source of food supply. Hence the light is another factor concerned

with the distribution of free-living Protozoa. Chemical composition of water. The chemical nature of the water is another important factor which influences the very existence of Protozoa in a given body of water. Protozoa differ from one another in morphological as well as physiological characteristics. Individual

protozoan species requires a certain chemical composition of the water in which it can be cultivated under experimental conditions, although this may be more or less variable among different forms

(Needham

et

al, 1937).

In their "biological analysis of water" Kolkwitz and Marsson (1908, 1909) distinguished four types of habitats for many aquatic

and a few animal, organisms, which were based upon the kind and amount of inorganic and organic matter and amount of oxygen
plant,

present in the water: namely, katharobic, oligosaprobic, mesosapro-

and polysaprobic. Katharobic protozoans are those which live in mountain springs, brooks, or ponds, the water of which is rich in oxygen, but free from organic matter. Oligosaprobic forms are those that inhabit waters which are rich in mineral matter, but in which no purification processes are taking place. Many Phytomastigina, various testaceans and many ciliates, such as Frontonia, Lacrymaria,
bic,

Oxytricha, Stylonychia, Vorticella, etc. inhabit such waters.

Meso-

saprobic protozoans live in waters in which active oxidation and de-

composition of organic matter are taking place. The majority of freshwater protozoans belong to this group: namely, numerous
Phytomastigina, Heliozoa, Zoomastigina, and
all

orders of Ciliata.

Finally polysaprobic forms are capable of living in waters which,

because of dominance of reduction and cleavage processes of organic matter, contain at most a very small amount of oxygen and are rich in carbonic acid gas and nitrogenous decomposition products. The
black bottom slime contains usually an abundance of ferrous sulphide and other sulphurous substances. Lauterborn (1901) called this
sapropelic.
palustris,

Examples of polysaprobic protozoans are Pelomyxa Euglypha alveolata, Pamphagus armatus, Mastigamoeba, Trepomonas agilis, Hexamita inflata, Rhynchomonas nasuta, Heteronema acus, Bodo, Cercomonas, Dactylochlamys, Ctenostomata, etc. The so-called "sewage organisms" abound in such habitat (Lackey,
1925).

Certain free-living Protozoa which inhabit waters rich in decom-

24

PROTOZOOLOGY

posing organic matter are frequently found in the faecal matter of

various animals. Their cysts either pass through the alimentary

canal of the animal

infusion.

unharmed or

are introduced after the faeces are

voided, and undergo development and multiplication in the faecal

Such forms are

rich in

collectively called coprozoic Protozoa.

The

coprozoic protozoans grow easily in suspension of old faecal matter

which

is

decomposed organic matter and thus show a

strik-

ingly strong capacity of adapting themselves to conditions different

from those of the water in which they normally live. Some of the Protozoa which have been referred to as coprozoic and which are mentioned in the present work are, as follows: Scytomonas pusilla, Rhynchomonas nasuta, Cercomonas longicauda, C. crassicauda, Trepomonas agilis, Naegleria gruberi, Acanthamoeba hyalina, Chlamydophrys stercorea and Tillina magna. As a rule, the presence of sodium chloride in the sea water prevents the occurrence of numerous species of fresh-water inhabitants. Certain species, however, have been known to live in both fresh and brackish or salt water. Among the species mentioned in the present work, the following species have been reported to occur in both fresh and salt waters: Mastigophora: Amphidinium lacustre, Ceratium hirundinella; Sarcodina: Lieberkiihnia wagneri; Ciliata: Mesodinium pidex, Prorodon discolor, Lacrymaria olor, Amphileptus claparedei, Lionotus fasciola, Nassula aurea, Trochilioides recta, Chilodonella cucullulus, Trimyema compressum, Paramecium calkinsi, Colpidium campylum, Platynematum sociale, Cinetochilum margaritaceum, Pleuronema coronatum, Caenomorpha medusula, Spirostomum minus, S. teres, Climacostomum virens, and Thuricola folliculata; Sxictoria, Metacineta mystacina, Endosphaera engelmanni. It seems probable that many other protozoans are able to live in both fresh and salt water, judging from the observations such
:

made by Finley (1930) who subjected some fifty species of freshwater Protozoa of Wisconsin to various concentrations of sea
as that

by gradual addition of the sea Uronema marinum, Pleuronema jaculans and Colpoda aspera are able to live and reproduce even when directly transferred to sea water, that Amoeba verrucosa, Euglena, Phacus, Monas, Cyclidium, Euplotes, Lionotus, Paramecium, Stylonychia, etc., tolerate only a low salinity when directly
water, either
water.
direct transfer or

by

He found

that Bodo uncinatus,

transferred, but,

if

the salinity

is

gradually increased, they live in

etc.

100 per cent sea water, and that Arcella, Cyphoderia, Aspidisca, Ble-

pharisma, Colpoda cucullus, Halteria,

cent sea water even

could not tolerate 10 per

gradual. Finley noted no

when the change was

ECOLOGY

25

morphological changes in the experimental protozoans which might

be attributed to the presence of the salt in the water, except Amoeba

which certain structural and physiological changes were observed as follows: as the salinity increased, the pulsation of the contractile vacuole became slower. The body activity continued up to 44 per cent sea water and the vacuole pulsated only once in 40 minutes, and after systole, it did not reappear for 10-15 minutes. The organism became less active above this concentration and in 84 per cent sea water the vacuole disappeared, but there was still a tendency to form the characteristic ridges, even in 91 per cent sea
verrucosa, in

water, in which the organism was less fan-shaped and the cytoplasm seemed to be more viscous. Yocom (1934) found that Ewplotes patella was able to live normally and multiply up to 66 per cent of sea water; above that concentration no division was noticed, though the organism lived for a few days in up to 100 per cent salt water, and Paramecium caudatum and Spirostomum ambiguum were less adaptive to salt water, rarely living in 60 per cent sea water. Frisch (1939) found that no freshwater Protozoa lived above 40 per cent sea water and that Paramecium caudatum and P. multimicronucleatum died in 33-52 per cent sea water. Hardin (1942) reports that Oikomonas termo will grow when transferred directly to a glycerolpeptone culture medium, in up to 45 per cent sea water, and cultures contaminated with bacteria and growing in a dilute glycerol-peptone medium will grow in 100 per cent sea water. Hydrogen-ion concentration. Closely related to the chemical composition is the hydrogen-ion concentration (pH) of the water. Some Protozoa appear to tolerate a wide range of pH. The interesting proteomyxan, Leptomyxa reticulata, occurs in soil ranging in pH 4.3 to 7.8, and grows very well in non-nutrient agar between pH 4.2 and
8.7,

provided a suitable bacterial strain

;

is

supplied as food (Singh,

1948) and according to Loefer and Guido (1950), a strain of Euglena

gracilis (var. bacillaris)

grows between pH 3.2 and 8.3. However, the majority of Protozoa seem to prefer a certain range of pH for the

maximum

metabolic activity.
of freshwater bodies varies a great

The hydrogen-ion concentration

deal between highly acid bog waters in which various testaceans

may frequently be present, to highly alkaline water in which such forms as Acanthocystis, Hyalobryon, etc., occur. In standing deep fresh water, the bottom region is often acid because of the decomposing organic matter, while the surface water is less acid or slightly alkaline due to the photosynthesis of green plants which utilize carbon dioxide. In some cases different pH may bring about morpho-


26
logical differences.

PROTOZOOLOGY
in

For example, in bacteria-free cultures of Paraa tryptone medium, Loefer (1938) found that at pH 7.6-8.0 the length averaged 86 or 87/x, but at 6.0-6.3 the length was about 129/z. The greatest variation took place at pH 4.6 in which no growth occurred. The shortest animals at the acid and alkaline extremes of growth were the widest, while the narrowest forms (about 44m wide) were found in culture at pH 5.7-7.4. Many workers have made observations on the pH range of the water or medium in which certain protozoans live, grow, and multiply, some of which

mecium bursaria

data are collected

in
1
.

Table

Table

Protozoa and hydrogen-ion concentration

Protozoa

28

PROTOZOOLOGY

not yet been comprehended. Certain strains of bacteria were found by Hardin (1944) to be toxic for Paramecium multimicronucleatum,

but if Oikomonas termo was present in the culture, the ciliate was maintained indefinitely. This worker suggested that the flagellate may be able to "detoxify" the metabolic products produced by the bacteria. Food relation in ciliates (Faure-Fremiet, 1950, 1951a). The adaptability of Protozoa to varied environmental conditions influences their distribution. The degree of adaptability varies a great deal, not only among different species, but also among the individuals of the same species. Stentor coeruleus which grows ordinarily under nearly anaerobic conditions, is obviously not influenced by alkalinity, pH, temperature or free carbon dioxide in the water
(Sprugel, 1951).

Some protozoans inhabit soil of various types and localities. Under ordinary circumstances, they occur near the surface, their maximum abundance being found at a depth of about 10-12 cm. (Sandon,
1927). It
is

said that a very few protozoans occur in the subsoil.

Here

also one notices a very

wide geographical distribution

of ap-

parently one and the same species. For example, Sandon found Amoeba proteus in samples of soil collected from Greenland, Tristan
Argentina. This

da Cunha, Gough Island, England, Mauritius, Africa, India, and amoeba is known to occur in various parts of North America, Europe, Japan, and Australia. The majority of Testacea inhabit moist soil in abundance. Sandon observed Trinema enchelys
in the soils of Spitzbergen, Greenland,

England, Japan, Australia,

St.

Helena, Barbados, Mauritius, Africa, and Argentina.

Parasitic Protozoa

Some Protozoa belonging to all groups live on or in other organisms. The Sporozoa are made up exclusively of parasites. The relaand the protozoan differ in various ways, which make the basis for distinguishing the associations into three types as follows: commensalism, symbiosis, and parasitism. Commensalism is an association in which an organism, the comtionships between the host

mensal,

is

benefited, while the host

is

neither injured nor benefited.

Depending upon the location of the commensal in the host body, the term ectocommensalism or endocommensalism is used. Ectocommensalism is often represented by Protozoa which may attach themselves to any aquatic animals that inhabit the same bod}' of water, as shown by various species of Chonotricha, Peritricha, and Suctoria. In other cases, there is a definite relationship between the commensal and the host. For example, Kerona polyporum is found

ECOLOGY
on various species of
mussels.

29
ciliates

Hydra, and

many

placed in Thigmo-

tricha (p. 774) are inseparably associated with certain species of

Endocommensalism

is

often difficult to distinguish from endo-

parasitism, since the effect of the presence of a

commensal upon the

host cannot be easily understood.

On

the whole, the protozoans

which live in the lumen of the alimentary canal may be looked upon as endocommensals. These protozoans undoubtedly use part of the food material which could be used by the host, but they do not invade the host tissue. As examples of endocommensals may be mentioned:

Endamoeba

blattae,

Lophomonas

blattarum,
coli,

L.

striata,

Nyctotherus ovalis,
biitschlii,

etc., of

the cockroach; Entamoeba

Iodamoeba

nili, etc., of

Endolimax nana, Dientamoeba fragilis, Chilomastix mesthe human intestine; numerous species of Protociliata of Anura, etc. Because of the difficulties mentioned above, the term parasitic Protozoa, in its broad sense, includes the commenals also. Symbiosis on the other hand is an association of two species of organisms, which is of mutual benefit. The cryptomonads belonging to Chrysidella ("Zooxanthellae") containing yellow or brown chromatophores, which live in Foraminifera and Radiolaria, and certain
belonging to Chlorella ("Zoochlorellae") containing green chromatophores, which occur in some freshwater protozoans, such as Paramecium bursaria, Stentor amethystinus, etc., are looked upon as holding symbiotic relationship with the respective protozoan host. Several species of the highly interesting Hypermastigina, which are
algae

and by Cleveland to digest the cellulose material which makes up the bulk of woodchips the host insects take in and to transform it into glycogenous substances that are used partly by the host insects. If deprived of these flagellates by being subjected to oxygen under pressure or to
present

commonly and abundantly

in various species of termites

the woodroach Cryptocercus, have been demonstrated

a high temperature, the termites

filled

with wood-chips.

If

die, even though the intestine is removed from the gut of the termite, the

perish (Cleveland, 1924, 1925). Recently, Cleveland (1949-1950c) found that the molting hormone produced by Cryptocercus induces sexual reproduction in several flagellates inhabiting its hind-gut (p. 185). Thus the association here may be said to be an
flagellates

absolute symbiosis.

Parasitism
lives at the

is

an association in which one organism (the parasite)

.

expense of the other (the host) Here also ectoparasitism and endoparasitism occur, although the former is not commonly found. Hydramoeba hydroxena (p. 464) feeds on the body cells of

.30

PROTOZOOLOGY

Hydra which, according to Reynolds and Looper (1928), die on an average in 6.8 days as a result of the infection and the amoebae disappear in from 4 to 10 days if removed from a host Hydra. Costia
necatrix (p. 372) often occurs in an

enormous number, attached to

various freshwater fishes especially in an aquarium, by piercing

through the epidermal

cells

and appears to disturb the normal funcfishes,

tions of the host tissue. Ichthyophthirius multifiliis (p. 709), another

ectoparasite of freshwater
tissue cells

pletely burying themselves in the epidermis

goes further by comand feeds on the host's and, not infrequently, contributes toward the cause of the
fishes.

and marine

death of the host

The endoparasites absorb by osmosis the vital body fluid, feed on the host cells or cell-fragments by pseudopodia or cytostome, or
enter the host tissues or
in
cells

themselves, living on the cytoplasm or

some cases on the nucleus. Consequently they bring about abnormal or pathological conditions upon the host which often succumbs to the infection. Endoparasitic Protozoa of man are Entamoeba histolytica, Balantidium coli, species of Plasmodium and Leishmania, Trypanosoma gambiense, etc. The Sporozoa, as was stated before, are
without exception coelozoic, histozoic, or cytozoic parasites. Because of their modes of living, the endoparasitic Protozoa cause certain morphological changes in the cells, tissues, or organs of the host. The active growth of Entamoeba histolytica in the glands of the colon of the victim, produces first slightly raised nodules which develop into abscesses and the ulcers formed by the rupture of abscesses, may reach 2 cm. or more in diameter, completely destroying
the tissues of the colon wall. Similar pathological changes

may

also

occur in the case of infection by Balantidium coli. In Leishmania donovani, the victim shows an increase in number of the large macro-

phages and mononuclears and also an extreme enlargement of the Trypanosoma cruzi brings about the degeneration of the infected host cells and an abundance of leucocytes in the infected tissues, followed by an increase of fibrous tissue. T. gambiense, the causative organism of African sleeping sickness, causes enlargement of lymphatic glands and spleen, followed by changes in meninges and an increase of cerebro-spinal fluid. Its most characteristic changes are the thickening of the arterial coat and the round-celled
spleen.
infiltration

around the blood vessels

is

of the central

nervous system.

Malarial infection

invariably accompanied

by an enormous

enlargement of the spleen ("spleen index"); the blood becomes watery; the erythrocytes decrease in number; the leucocytes, subnormal; but mononuclear cells increase in number; pigment granules

ECOLOGY
which are
set free in the blood

31

plasma at the time of merozoiteby leucocytes; and enlarged spleen contains large amount of pigments which are lodged in leucocytes and endothelial cells. In Plasmodium falciparum, the blood capillaries of brain, spleen and other viscera may completely be blocked by inliberation are engulfed

fected erythrocytes.

In Myxosporidia which are either histozoic or coelozoic parasites

of fishes, the tissue cells that are in direct contact

with highly en-

larging parasites, undergo various morphological changes. For

exam-

fEssssxgsss

''

'i**i?<

'::

-X^^<:

?-:

m .&?: %: %m
Histological changes in host fish caused by myxosporidian inof a cyst of Myxobolus intestinalis, surof the black crappie; b, part of a cyst of Thelohanellus notatus, enveloped by the connective tissue of the bluntFig.
1.

X1920 (Kudo), a, portion rounded by peri-intestinal muscle

fection,

nosed minnow.
pie,

the circular muscle fibers of the small iniestine of Pomoxis

which surround Myxobolus intestinalis, a myxosporidian, become modified a great deal and turn about 90 from the original direction, due undoubtedly to the stimulation exercised by the myxosporidian parasite (Fig. 1, a). In the case of another myxosparoides,

sporidian, Thelohanellus notatus, the connective tissue cells of the

host fish surrounding the protozoan body, transform themselves into

"epithelial cells" (Fig.
1, b),

a state comparable to the formation of

the ciliated epithelium from a layer of fibroblasts lining a cyst

formed around a piece of ovary inplanted into the adductor muscle of Pecten as observed by Drew (1911),

32

PROTOZOOLOGY

Practically all Microsporidia are cytozoic, and the infected cells become hypertrophied enormously, producing in one genus the socalled

Glugea cysts

(Figs. 287, 290). In

is

many cases,

the hypertrophy

of the nucleus of the infected cell of the

far

more conspicuous than that

cytoplasm (Figs. 287, 291) (Kudo, 1924). the gonads are parasitized heavify, the germ cells of the host animal often do not develop, thus resulting in parasitic castration. For example, the ciliate, Orchitophrya steUarum, a parasite in the male reproductive organ of Asterias rubens, was found by Vevers (1951) to break down completely all germinal tissues of the testes in the majority of the host starfish. In other cases, the protozoan does not invade the gonads, but there is no development of the germ cells. The microsporidian, Nose ma apis, attacks solely the gut epithelium of the honey bee, but the ovary of an infected queen bee degenerates to varying degrees (Hassanein, 1951). Still in other instances, the Protozoa invade developing ova of the host, but do not hinder their development, though the parasites multiply, as in Nosema bombycis in the silkworm (Stempell, 1909) and Babesia bigemina in the cattle

When

tick (Dennis, 1932).

For the great majority

finite

of parasitic Protozoa,

there exists a de-

and animals other than the specific hosts possess a natural immunity against an infection by a particular parasitic protozoan. Immunity involved in diseases caused by Protozoa has been most intensively studied on haemozoic forms, especially Plasmodium and Trypanosoma, since they are the causative organisms of important diseases. Development of these organisms in hosts depends on various factors such as the species and strains of the parasites, the species and strains of vectors, and immunity of the host. Boyd and co-workers showed that reinoculation of persons who have recovered from an infection with Plasmodium vivax or P. falciparum with the same strain of the parasites, will not result in a second clinical attack, because of the development of homologous immunity, but with a different strain of the same species or different species, a definite clinical attack occurs, thus there being no heterologous tolerance. The homologous immunity was found to continue for at least three years and in one case for about seven years in P. vivax, and for at least four months in P. falciparum after apparent
host-parasite relationship

eradication of the infection. In the case of leishmaniasis, recovery

from a natural or induced infection apparently develops a lasting immunity against reinfection with the same species of Leishmania. It has been shown that in infections with avian, monkey and hu-

man Plasmodium

or

Trypanosoma hwisi a considerable number

1

of

ECOLOGY
infection

33

the parasites are destroyed during the developmental phase of the

and that

after a variable length of time, resistance to the

parasites often develops in the host, as the parasites disappear from

the peripheral blood and

symptoms

subside,

though the host

still

harbors the organisms. In malarious countries, the adults and chilively,

dren show usually a low and a high rate of malaria infection respectbut the latter frequently do not show symptoms of infection,

even though the parasites are detectable in the blood. Apparently repeated infection produces tolerance which can keep, as long as the host remains healthy, the parasites under control. There seems to be
also racial difference in the degree of immunity against Plasmodium and Trypanosoma. As to the mechanism of immunity, the destruction of the parasites by phagocytosis of the endothelial cells of the spleen, bone marrow and liver and continued regenerative process to replace the destroyed blood cells, are the two important phases in the cellular defense mechanism. Besides, there are indications that humoral defense mechanism through the production of antibodies is in active operation in infections by Plasmodium knowlesi and trypanosomes (Taliaferro, 1926; Maegraith, 1948; Culbertson, 1951). Immunity

(Taliaferro, 1941).

With regard
agreed

to the origin of parasitic Protozoa,

it

is

generally

among

biologists that the parasite in general evolved

from

the free-living form.

The protozoan association with other organisms was begun when various protozoans which lived attached to, or by crawling on, submerged objects happened to transfer themselves to various invertebrates which occur in the same water. These Protozoa benefit by change in location as the host animal moves about, and thus enlarging the opportunity to obtain a continued supply of food material. Such ectocommensals are found

abundantly; for example, the peritrichous ciliates attached to the body and appendages of various aquatic animals such as larval insects

and microcrustaceans. Ectocommensalism

may

next lead to

ectoparasitism as in the case of Costia or Hydramoeba, and then

again instead of confining themselves to the body surface, the Pro-

tozoa

may bore

into the

body wall from outside and actually acquire

cells of

the habit of feeding on tissue

case of Ichthyophthirius.

the attached animals as in the

The next step in the evolution of parasitism must have been reached when Protozoa, accidentally or passively, were taken into the digestive system of the Metazoa. Such a sudden change in
habitat appears to be fatal to most protozoans.

But

certain others

34

PROTOZOOLOGY

an entirely For example, Dobell (1918) observed in the tadpole gut, a typical free-living limax amoeba, with characteristic nucleus, contractile vacuoles, etc., which was found in numbers in the water containing the faecal matter of the tadpole. Glaucoma (Tetrahymena) pyriformis, a free-living ciliate, was found to occur
possess extraordinary capacity to adapt themselves to
different environment.
in the

body cavity of the larvae of Theobaldia annulata (after MacArthur) and in the larvae of Chironomus plumosus (after Treillard and Lwoff). Lwoff successfully inoculated this ciliate into the larvae of Galleria mellonella which died later from the infection. Janda and Jirovec (1937) injected bacteria-free culture of this ciliate into annelids, molluscs, crustaceans, insects, fishes, and amphibians, and found that only insects all of 14 species (both became infected by this ciliate. In a few days larvae and adults) after injection the haemocoele became filled with the ciliates. Of various organs, the ciliates were most abundantly found in the

adipose tissue.
jected,

in the original culture.

The organisms were much larger than those present The insects, into which the ciliates were indied from the infection in a few days. The course of developof the culture injected,

an experimental insect depended not only but also on the temperature. At 1-4C. the development was much slower than at 26C; but if an infected insect was kept at 32-36C. for 0.5-3 hours, the ciliates were apparently killed and the insect continued to live. When Glaucoma taken from Dixippus morosus were placed in ordinary water, they continued to live and underwent multiplication. The ciliate showed a remarkable power of withstanding the artificial digestion; namely, at 18C. they lived 4 days in artificial gastric juice with pH 4.2; 2-3 days in a juice with pH 3.6; and a few hours in a juice with pH 1.0. Cleveland (1928) observed Tritrichomonas fecalis in faeces of a single human subject for three years which grew well in faeces diluted with tap water, in hay infusions with or without free-living protozoans or in tap water with tissues at 3 to 37C, and which, when fed per os, was able to live indefinitely in the gut of frogs and tadpoles. Reynolds (1936) found that Colpoda steini, a free-living ciliate of fresh water, occurs naturally in the intestine and other viscera of the land slug, Agriolimax agrestis, the slug forms being much larger than the free-living individuals. It may be further speculated that Vahlkampfia, Hydramoeba, Schizamoeba, and Endamoeba, are the different stages of the course the intestinal amoebae might have taken during their evolution. Obviously endocommensalism in the alimentary canal was the initial phase of endoparasitjsm. When these endocommensals began
of the ciliate within

ment

on the amount

ECOLOGY
to
of the host gut,

35

consume an excessive amount of food or to feed on the tissue cells they became the true endoparasites. Destroying or penetrating through the intestinal wall, they became first established in the body or organ cavities and then invaded tissues, cells or even

The endoparasites developing in invertebrates which feed upon the blood of vertebrates as source of food supply, will have opportunities to establish themnuclei, thus developing into pathogenic Protozoa.

selves in the higher animals.

parasitize other protozoan or

Hyperparasitism. Certain parasitic Protozoa have been found to metazoan parasites. This association is
hyperparasitism. The microsporidian

named
672)
is

Nosema

notabilis (p.

an exclusive parasite of the myxosporidian Sphaerospora polymorpha, which is a very common inhabitant of the urinary bladder of the toad fish along the Atlantic and Gulf coasts. A heavy infection of the microsporidian results in the degeneration and death of the host myxosporidian trophozoite (Kudo, 1944). Thus Nosema notabilis is a hyperparasite. Organisms living on and in Protozoa (Duboscq and Grasse, 1927, 1929; Georgevitch, 1936; Grasse, 1936;
Kirby, 1932, 1938, 1941, 1941a, 1942, 1942a, 1942b, 1944, 1946)

References

Bland,

P. B., Goldstein, L., Wenrich, D. H. and Weiner, Eleanor: (1932) Studies on the biology of Trichomonas vaginalis.
J.

Am.

Hyg., 56:492.
:

Chalkley, H. W. (1930) Resistance of Paramecium to heat as affected by changes in hydrogen-ion concentration and in inorganic salt balance in surrounding medium. U. S. Pub. Health,
Rep., 45:481.

Chambers, R. and Hale, H.

:

P.: (1932) The formation of ice in protoplasm. Proc. Roy. Soc. London, Ser. B, 110:336. Cleveland, L. R. (1924) The physiological and symbiotic relationships between the intestinal protozoa of termites and their host, with special reference to Reticulitermes flavipes Kollar. Biol. Bull., 46:177. (1925) The effects of oxygenation and starvation on the symbiosis between the termite, Termopsis, and its intestinal flagellates. Ibid., 48:309. (1926) Symbiosis among animals with special reference to termites and their intestinal flagellates. Gen. Rev. Biol., 1:51. (1928) Tritrichomonas fecalis nov. sp. of man, etc. Amer. J. Hyg., 8:232. (1949) Hormone-induced sexual cycles of flagellates. I. Jour. Morph., 85:197. - (1950) II. Ibid., 86:185. - (1950a) III. Ibid., 86:215. - (1950b) IV. Ibid, 87:317. (1950c) V. Ibid, 87:349.

36

PROTOZOOLOGY
:

L. T. (1939) Preservation of viable malaria parasites in the frozen state. Proc. Soc. Exp. Biol., 42:499. Oulbertson, J. T. (1951) Immunological mechanisms in parasitic. York. infections. In: Most's Parasitic infections in man. Dallinger, W. H.: (1887) The president's address. J. Roy. Micro.

Coggeshall,

New

Soc, London, 7:185.

Darby, H. H.: (1929) The

:

effect of the hydrogen-ion concentration on the sequence of protozoan forms. Arch. Protist., 65:1. Dennis, E. W. (1932) The life-cycle of Babesia bigemina, etc., Univ.

Cal. Publ. Zoology, 36:263.

Deschiens, R. (1934) Influence du froid sur les formes vegetatives de ramibe dysenterique. C. R. Soc. Biol., 115:793. Dobell, C. (1918) Are Entamoeba histolytica and E. ranarum the same species? Parasit., 10:294. Doudoroff, M.: (1936) Studies in thermal death in Paramecium. J.
: :

Drew, G.

Exper. Zool., 72:369. H.: (1911) Experimental metaphasia. 10:349.

I. J.

Exper. Zool.,

Duboscq, O. and Grasse,

P.: (1927) Flagelles et Schizophytes de Calotermes (Glyptotermes) iridipennis. Arch. zool. exp. gen., 66: 451. (1929) Sur quelques protistes d'un Calotermes, etc. Ibid., 68:8. Efimoff, W. W. (1924) Ueber Ausfrieren und Ueberkaeltung der Protozoen. Arch. Protist., 49: 431. Fatjre-Fremiet, E.: (1950) Ecology of ciliate infusoria. Endeavour 9, 3 pp. (1951) The marine sand-dwelling ciliates of Cape Cod. Biol. Bull., 100:59. (1951a) Ecologie des Protistes littoraux. Ann. Biol., 27:205. Finley, H. E. (1930) Toleration of freshwater Protozoa to increased salinity. Ecology, 11:337. Frisch, J. A.: (1939) The experimental adaptation of Paramecium to sea water. Arch. Protist., 93:38. Gaylord, H. R.: (1908) The resistance of embryonic epithelium, etc. J. Infect. Dis., 5:443. Georgevitch, J.: (1936) Ein neuer Hyperparasit, Leishmania esocis n. sp. Arch. Protist., 88:90. Glaser, R. W. and Coria, N. A.: (1933) The culture of Paramecium caudatum free from living microorganisms. Jour. Parasit., 20:
: :

33.

Am.
J.

(1935)

The

culture

and reactions

of purified Protozoa.

Hyg,

21:111.

Grasse, P.

P.: (1938) La veture schizophytique des flagelles termiticoles, etc. Bull. Soc. zool. France, 63:110. Greeley, A. W. (1902) On the analogy between the effects of loss of water and lowering of temperature. Amer. Jour. Physiol., 6:
:

122.

Hardin, G. (1944) Symbiosis

:

of

Paramecium and Oikomonas. Ecol-

ogy, 25:304.

ECOLOGY
:

37

Hassanein, M. H. (1951) Studies on the effect of infection with Nosema apis on the physiology of the queen honey-bee. Quart. J. Micr. Sc, 92:225. Howland, Ruth: (1930) Micrurgical studies on the contractile vacuole. III. J. Exper. Zool., 55:53.

(1933) Studies on the physiology of the euglenoid flagIV. Arch. Protist., 79:249. Janda, V. and Jirovec, O. (1937) Ueber kiinstlich hervorgerufenen Parasitismus eines freilebenden Ciliaten Glaucoma piriformis, etc. Mem. Soc. Zool. Tehee. Prague, 5:34. Kidder, G. W.: (1941) Growth studies on ciliates. VII. Biol. Bull, 80:50. Kirby, H. Jr.: (1932) Flagellates of the genus Trichonympha in termites. Univ. Cal. Publ. Zool., 37:349. (1938) The devescovinid flagellates, etc. Ibid., 43:1. (1941) Devescovinid flagellates of termites. I. Ibid., 45:1. (1941a) Organisms living on and in Protozoa. Calkins and Summers' Protozoa in biological research. (1942) Devescovinid flagellates of termites. II. Uni. Cal. Publ. Zool., 45:93. (1942a) III. Ibid., 45:167. (1942b) A parasite of the macronucleus of Vorticella. Jour. Parasit., 28:311. (1944) The structural characteristics and nuclear parasites of some species of Trichonympha in termites. Uni. Cal. Publ. Zool., 49:185. (1946) Gigayitomonas herculea, etc. Ibid., 53:163. Klebs, G.: (1893) Flagellatenstudien. Zeitschr. wiss. Zool, 55: 265. Kolkwitz, R. and Marsson, M.: (1909) Oekologie der tierischen Sabrobien. Intern. Rev. Ges. Hydrobiol. u. Hydrogr., 2:126. Kudo, R. R. (1924) A biologic and taxonomic study of the Microsporidia. Illinois Biol. Monogr., 9: nos. 3 and 4. (1929) Histozoic Myxosporidia found in freshwater fishes of Illinois, U. S. A. Arch. Protist., 65:364. (1944) Morphology and development of Nosema notabilis Kudo, parasitic in Sphaerospora polymorpha Davis, a parasite of Opsanus tau and 0. beta. Illinois Biol. Monogr., 20:1. Kuhne, W. (1864) Untersuchungen ueber das Protoplasma und die

Jahn, T. L.
ellates.

Contractilitat. Leipzig. Lackey, J. B.: (1925) The fauna of Imhof tanks. Bull. N. J. Agr. Ex. St., No. 417. Lauterborn, R. (1901) Die "sapropelische" Lebewelt. Zool. Anz.,
:

24:50.

Loefer, J. B.: (1935) Relation of hydrogen-ion concentration to growth of Chilomonas and Chlorogonium. Arch. Protist., 85:
209. (1938) Effect of hydrogen-ion concentration on the growth and morphology of Paramecium bursaria. Ibid., 90:185. (1939) Acclimatization of fresh- water ciliates and flagellates to media of higher osmotic pressure. Physiol. Zool., 12:161,

38

PROTOZOOLOGY
Euglena

and Guido, Virginia M.: (1950) Growth and survival of gracilis, etc. Texas J. Sc, 2:225. Luyet, B. J. and Gehenio, P. M.: (1940) The mechanism of injury and death by low temperature. A review. Biodynamica, 3: no.
60.

in malaria and blackwater fever. Springfield, Illinois. Molisch, H. (1897) Untersuchungen ueber das Erfrieren der Pflan: :

Maegraith, B. (1948) Pathological processes

zen. Jena. Needhum, J. G.,

Galtsoff, P. S., Lutz, F. E. and Welch, (1937) Culture methods for invertebrate animals. Ithaca, Noland, L. E.: (1925) Factors influencing the distribution of water ciliates. Ecology, 6:437. Phelps, A.: (1934) Studies on the nutrition of Paramecium.
Protist., 82:134.
:

P. S.:

N. Y.
fresh-

Arch.

Reynolds, B. D. (1936) Colpoda

steini, a facultative parasite of the land slug, Agriolimax agrestis. J. Parasit., 22:48. and Looper, J. B. (1928) Infection experiments with Hydramoeba hydroxena nov. gen. Ibid., 15:23. Rosenberg, L. E.: (1936) On the viability of Trichomonas augusta. Tr. Am. Micr. Soc, 55:313. Sandon, H. (1927) The composition and distribution of the protozoan fauna of soil. Edinburgh. Schoenborn, H. W. (1950) Nutritional requirements and the effect of pH on growth of Euglena viridis in pure culture. Tr. Am. Micr. Soc, 69:217. Singh, B. N. (1948) Studies on giant amoeboid organisms. I. J. Gen.

Microbiol., 2:7. Sprugel, G., Jr.: (1951) Vertical distribution of Stentor coeruleus in relation to dissolved oxygen levels in an Iowa pond. Ecology,

32:147.

Stempell, W.
281.

(1909)

Ueber Nosema bombycis. Arch.

Protist., 16:

Taliaferro, W. H.: (1926) Host resistance and types of infections in trypanosomiasis and malaria. Quart. Rev. Biol., 1:246.

in Japan. IV. Ecolog. St., 2:171. Rep. Japan. Sc. A., 12:264. (1937) V. Vevers, H. G.: (1951) The biology of Asterias rubens. II. J. Mar. Biol. A. Un. Kingd. 29:619. Wichterman, R. (1948) The hydrogen-ion concentration in the cultivation and growth of 8 species of Paramecium. Biol. Bull., 95:271. Wolfson, C. (1935) Observations on Paramecium during exposure to sub-zero temperatures. Ecology, 16:630. Yocom, H. B.: (1934) Observations on the experimental adaptation of certain freshwater ciliates to sea water. Biol. Bull, 67:273.

The immunology of the parasitic Protozoa. and Summers' Protozoa in biological research. Uyemura, M.: (1936) Biological studies of thermal waters
(1941)
ins

In: Calk-

Chapter

Morphology
range in size from submicroscopic to macroscopic, though they are on the whole minute microscopic animals. The parasitic forms, especially cytozoic parasites, are often extremely small, while free-living protozoans are usually of much larger dimensions. Noctiluca, Foraminifera, Radiolaria, many ciliates such as
Stentor, Bursaria,
etc.,

PROTOZOA

represent larger forms.

Colonial protoetc.,

zoans such as Carchesium, Zoothamnium, Ophrj^dium,

greater than the solitary forms.
ples of the smallest forms.

are even

On

the other hand, Plasmodium,

Leishmania, and microsporidian spores

may

be mentioned as exam-

The

unit of measurement employed in

protozoology
equal to 0.001
its

is,

as in general microscopy, 1 micron (n)

which

is

mm.

of Protozoa is even more varied, and because of extreme plasticity it frequently does not remain constant. Furthermore the form and size of a given species may vary according to the kind and amount of food as is discussed elsewhere (p. 109). From a small simple spheroidal mass up to large highly complex forms, all possible body forms occur. Although the great majority are without symmetry, there are some which possess a definite symmetry. Thus bilateral symmetry is noted in all members of Diplomonadina (p.

The body form

392); radial

symmetry in Gonium, Cyclonexis, etc.; and universal symmetry, in certain Heliozoa, Vol vox, etc. The fundamental component of the protozoan body is the protoplasm which is without exception differentiated into the nucleus and the cytoplasm. Haeckel's (1868, 1870) monera are now considered as nonexistent, since improved microscopic technique has failed in recent years to reveal any anucleated protozoans. The nucleus and the cytoplasm are inseparably important to the well-being of a protozoan, as has been shown by numerous investigators since Verworn's
pioneer work. In
all cases,

successful regeneration of the

body

is

ac-

complished only by the nucleus-bearing portions and enucleate parts degenerate sooner or later. On the other hand, when the nucleus is taken out of a protozoan, both the nucleus and cytoplasm degenerate, which indicates their intimate association in carrying on the
activities of the

body.

It

appears certain that the nucleus controls

the assimilative phase of metabolism which takes place in the cyto-

plasm in normal animals, while the cytoplasm is capable of carrying on the catabolic phase of the metabolism. Aside from the importance
39

40

PROTOZOOLOGY

as the controlling center of metabolism, evidences point to the con-

clusion that the nucleus contains the genes or hereditary factors

which characterize each species

of

Protozoa from generation to gen-

eration, as in the cells of multicellular animals

and

plants.

The nucleus
Because of a great variety of the body form and organization, the protozoan nuclei are of various forms, sizes and structures. At one extreme there is a small nucleus and, at the other, a large voluminous

one and, between these extremes, is found almost every conceivable variety of form and structure. The majority of Protozoa contain a single nucleus, though many may possess two or more throughout the greater part of their life-cycle. In several species, each individual possesses two similar nuclei, as in Diplomonadina, Protoopalina and Zelleriella. In Euciliata and Suctoria, two dissimilar nuclei, a macronucleus and a micronucleus, are typically present. The macronucleus is always larger than the micronucleus, and controls the
trophic activities of the organism, while the micronucleus
is

con-

cerned with the reproductive activity. Certain Protozoa possess

numerous nuclei

of similar structure, as for example, in Pelomyxa, Mycetozoa, Actinosphaerium, Opalina, Cepedea, Myxosporidia,

Microsporidia, etc.

components of the protozoan nucleus membrane, chromatin, plastin and nucleoplasm or nuclear sap. Their interrelationship varies sometimes from one developmental stage to another, and vastly among different species. Structurally, they fall in general into one of the two types: vesicular and compact. The vesicular nucleus (Fig. 2, a, c, e) consists of a nuclear memessential morphological

The

are the nuclear

is sometimes very delicate but distinct, nucleoplasm, achromatin and chromatin. Besides there is an intranuclear body which is, as a rule, more or less spherical and which appears to be of different make-ups as judged by its staining reactions among different nuclei. It may be composed of chromatin, of plastin, or of a mixture of both. The first type is sometimes called karyosome and the second, nucleolus or plasmosome. Absolute distinction between these two terms cannot be made as they are based solely upon the difference in affinity to nuclear stains which cannot be standardized and hence do not give uniformly the same result. Following Minchin (1912), the term endosome is advocated here to designate one or more conspicuous bodies other than the chromatin granules, present

brane which

within the nuclear

membrane

(Fig, 2, b, d).

Fig. 2. a-f, vesicular nuclei; g-j,

compact

nuclei,

X980.

a, b,
c,

nuclei of

Entamoeba invadens Amoeba spumosa (c,

nuclei of A. proteus
reaction)
;

(a,

in life; b, in stained organism);

life,

d,

nuclei of
f,

in
(e,

showing a large endosome;

f,

d, stained); e,

g,

a nucleus subjected to Feulgen's nucleal h, nuclei of Paramecium aurelia (g, in life under phase microin life;

scope, snowing

two vesicular micronuclei and compact macronucleus; h, Feulgen-stained nuclei); i, j, nuclei of Frontonia leucas, showing a micronucleus and macronucleus, both of which are compact ($ in life, showing many endosomes imbedded among the granules; j, nuclei stained with
acidified

methyl green),

42

PROTOZOOLOGY
When viewed
in
life,

and

the nucleoplasm is ordinarily homogeneous upon fixation, there appear invariably achromatic strands or networks which seem to connect the endosome and
structureless. But,

the nuclear

membrane

(Fig. 2,

b, d).

Some

investigators hold that

life,

but due to the simiand of the nucleoplasm, they are not visible and that, when fixed, they become readily recognizable because of a change in these indices. In some nuclei, however, certain strands have been observed in life, as for example in the nucleus of the species of Barbulanympha (Fig. 174, c), according to Cleveland and his associates (1934). Others maintain that the achromatic structures prominent in fixed vesicular nuclei are mere artifacts brought about by fixation and do not exist in life and that the nucleoplasm is a homogeneous liquid matrix of the nucleus in which
larity of refractive indices of the strands

these strands or networks exist naturally in

the chromatin

is

usually distributed as small granules. Frequently

and forms may occur along the inner membrane. These so-called peripheral granules that occur in Amoeba, Entamoeba, Pelomyxa, etc., are apparently not chromatinic (Fig. 2, a, e). The vesicular nucleus is most commonly present in various orders of Sarcodina and Mastigophora. The compact nucleus (Fig. 2, g-j), on the other hand, contains a large amount of chromatin substance and a comparatively small amount of nucleoplasm, and is thus massive. The macronucleus of the Ciliophora is almost always of this kind. The variety of forms of the compact nuclei is indeed remarkable. It may be spherical,
larger granules of various sizes

surface of the nuclear

ovate, cylindrical, club-shaped, band-form, moniliform, horseshoe-

form, filamentous, or dendritic.

distinct,

The nuclear membrane

is

is

always

and the chromatin substance

usually of spheroidal form,

varying in size
species. In the

among different species and often even in the same majority of species, the chromatin granules are small
i),

and compact

ovalis (Fig. 3),

some forms, such as Nyctotheru-s more in diameter in some individuals and while the smaller chromatin granules seem to be homo(Fig. 2, h,

though

in

they

may reach

20/x or

geneous, larger forms contain alveoli of different sizes in which

smaller chromatin granules are suspended (Kudo, 1936).
Precise knowledge of chromatin (thymo- or desoxyribose-nucleic
acid)
is still

lacking.

At present the determination

of the

depends upon the following

tests: (1) artificial digestion

chromatin which does

not destroy this substance, while non-chromatinic parts of the nucleus are completely dissolved; (2) acidified methyl green which
stains the chromatin bright green; (3) 10 per cent

solution which dissolves, or causes swelling

of,

sodium chloride chromatin granules,

MORPHOLOGY
while nuclear

43

membrane and achromatic substances remain unat-

tacked; and (4) in the fixed condition Feulgen's nucleal reaction (p. 897). Action of methyl green (Pollister and Leuchtenberger,
1949).

There

is

nuclei, since there are

no sharp demarcation between the vesicular and compact numerous nuclei the structures of which are

Fig.

3.

Parts of

nacronuclei of Nyctotherus ovalis, showing chromatin spherules of different sizes, X650 (Kudo).

intermediate between the two. Moreover what appears to be a

vesicular nucleus in
fixed
life, may approach a compact nucleus when and stained as in the case of Euglenoidina. Several experimental observations show that the number, size, and structure of the endosome in the vesicular nucleus, and the amount and arrangement of the chromatin in the compact nucleus, vary according to the physio-

logical state of the

whole organism. The macronucleus

may

be

44

PROTOZOOLOGY

divided into two or more parts with or without connections among them and in Dileptus anser into more than 200 small nuclei, each of

which

is

"composed

of

a plastin core and a chromatin cortex" (Cal-

kins; Hayes).

In a compact nucleus, the chromatin granules or spherules fill, as a rule, the intranuclear space compactly, in which one or more endosomes (Fig. 2, i) may occur. In many nuclei these chromatin granules

appear to be suspended freely, while in others a reticulum appears to make the background. The chromatin of compact nuclei gives a strong positive Feulgen's nucleal reaction. The macronuclear and micronuclear chromatin substances respond differently to Feulgen's nucleal reaction or to the so-called nuclear stains, as judged by the difference in the intensity or tone of color. In Paramecium caudatum., P. aurelia, Chilodonella, Nyctotherus ovalis, etc., the macronuclear chromatin is colored more deeply than the micronuclear chromatin, while in Colpoda, Urostyla, Euplotes, Stylonychia, and others, the reverse seems to be the case, which may support the validity of the assumption by Heidenhain that the two types of the nuclei of Euciliata and Suctoria are made up of different chromatin substances idiochromatin in the micronucleus and trophochromatin

in the

macronucleus and in other classes of Protozoa, the two kinds of chromatin are present together in a single nucleus. The macronucleus and the micronucleus of vegetative Paramecium caudatum were found by Moses (1950) to possess a similar nucleic acid-protein composition; namely, similar concentrations of total protein, nonhistone protein, desoxyribose nucleic acid and ribose nucleic acid.

Of the two latter nucleic acids, ribose nucleic acid is said to be present in a larger amount than desoxyribose nucleic acid in both nuclei. It may be considered that the two nucleic acids occur in different
proportions in the two nuclei. Chromidia. Since the detection of chromatin had solely depended

on

its affinity

to certain nuclear stains, several investigators found

extranuclear chromatin granules in

many

protozoans. Finding such

granules in the cytoplasm of Actinosphaerium eichhorni, Arcella vulgaris, and others, Hertwig (1902) called them chromidia, and maintained that under certain circumstances, such as lack of food
terial,

ma-

the nuclei disappear and the chromatin granules become scattered throughout the cytoplasm. In the case of Arcella vulgaris, the two nuclei break down completely to produce a chromidial-net

which later reforms into smaller secondary nuclei. It has, however, been found by Belaf that the lack of food caused the encystment rather than chromidia-formation in Actinosphaerium and, according

MORPHOLOGY

45

to Reichenow, Jollos observed that in Arcella the nuclei persisted,

but were thickly covered by chromidial-net which could be cleared

the two nuclei. In Diffiugia, the vacuolated or alveolated in the fall and in each alveolus appear glycogen granules which seem to serve as reserve food material for the reproduction that takes place during that

away by

artificial digestion to reveal

is

chromidial-net

season (Zuelzer), and the chromidia occurring in Actinosphaerium

appear to be of a combination of a carbohydrate and a protein (Rumjantzew and Wermel, 1925). Apparently the widely distributed volutin (p. 114), and many inclusions or cytozoic parasites, such as Sphaerita (p. 893), which occur occasionally in different Sarcodina, have in some cases been called chromidia. By using Feulgen's nucleal reaction, Reichenow (1928) obtained a diffused violet-stained zone in Chlamydomonas and held them to be dissolved volutin. Calkins (1933) found the chromidia of Arcella vulgaris negative to the nucleal reaction, but by omitting acid-hydrolysis and treating with fuchsinsulphurous acid for 8-14 hours, the chromidia and the secondary
nuclei were found to

show a

typical positive reaction

and believed

that the chromidia were chromatin.

of

Thus

at present the real nature

chromidia

is still

gists are inclined to

in

some way,

is

not clearly known, although many protozoolois not chromatinic, but, connected with the metabolism of the protozoan.
think that the substance

The cytoplasm
The extranuclear part
is

of the

composed

of a colloidal

system, which

protozoan body is the cytoplasm. It may be homogeneous, granu-

lated, vacuolated, reticulated, or fibrillar in optical texture,

and

is

almost always

colorless.

The chromatophore-bearing Protozoa

are

variously colored, and those with symbiotic algae or cryptomonads

are also greenish or brownish in color. Furthermore, pigment or

which are produced in the body may give protozoans various colorations. In several forms pigments are diffused throughout the cytoplasm. For example, many dinoflagellates are beautifully colored, which, according to Kofoid and Swezy, is due to a thorough diffusion of pigment in the cytoplasm. Stentor coeruleus is beautifully blue-colored. This coloration is due to the presence of pigment stentorin (Lankester, 1873) which occurs
crystals

as granules in the ectoplasm (Fig. 14).

The pigment
and
alkalis,

is

highly re-

sistant to various solvents such as acids

light does not affect its nature. It
is

and the sun-

destroyed by bleaching with

chlorine gas or with potassium permanganate, followed

by immer-

sion in 5 per cent oxalic acid (Weisz, 1948). Several species of Blepha-

46

PROTOZOOLOGY

risma are rose- or purple-colored. The color is due to the presence of zoopurpurin (Arcichovskij, 1905) which is lodged in numerous granules present in the ectoplasm. This pigment is soluble in alcohol, ether or acetone, and is destroyed by strong light (Giese, 1938). Weisz (1950) maintains that both pigment granules are chondriosomes, and in Stentor, cytochrome oxidase appears to be localized in
the pigment granules. The extent and nature of the cytoplasmic differentiation differ greatly among various groups. In the majority of Protozoa, the

cytoplasm is differentiated into the ectoplasm and the endoplasm. The ectoplasm is the cortical zone which is hyaline and homogeneous in Sarcodina and Sporozoa. In the Ciliophora it is a permanent and distinct part of the body and contains several organelles. The endoplasm is more voluminous and fluid. It is granulated or alveolated and contains various organellae. While the alveolated cytoplasm is normal in forms such as the members of Heliozoa and Radiolaria, in other cases the alveolation of normally granulated or vacuolated cytoplasm indicates invariably the beginning of degeneration of the protozoan body. In Amoeba and other Sarcodina, the "hyaline cap" and "layer" (Mast) make up the ectoplasm, and the "plasmasol" and "plamagel" (Mast) compose the endoplasm (Fig. 46). In numerous Sarcodina and certain Mastigophora, the body
is naked and not protected by any form-giving organella. However, the surface layer is not only elastic, but solid, and therefore the name plasma-membrane may be applied to it. Such forms are capable of undergoing amoeboid movement by formation of pseudopodia and by continuous change of form due to the movement of the cytoplasm which is more fluid. However, the majority of Protozoa possess a characteristic and constant body form due to the development of a special envelope, the pellicle. In Amoeba striata, A. verrucosa (Howland, 1924), Pelomyxa carolinensis, P. illinoisensis (Kudo, 1946, 1951), etc., there is a distinct pellicle. The same is true with some flagellates, such as certain species of Euglena, Peranema, and Astasia, in which it is elastic and expansible so that the organisms show a great deal of plasticity. The pellicle of a ciliate is much thicker and more definite, and often variously ridged or sculptured. In many, linear furrows and

surface

ridges run longitudinally, obliquely, or spirally; and, in others, the ridges are combined with hexagonal or rectangular depressed areas.
Still in others,
lel

to the longitudinal axis of the body.

ciliates,

such as Coleps, elevated platelets are arranged paralIn certain peritrichous such as Vorticella monilata, Carchesium granulatum, etc.,

MORPHOLOGY
the pellicle
parallel

47

may possess nodular thickenings arranged in more or less rows at right angles to the body axis. While the pellicle always covers the protozoan body closely, there are other kinds of protective envelopes produced by Protozoa which may cover the body rather loosely. These are the shell, test, lorica or envelope. The shell of various Phytomastigina is usually made up of cellulose, a carbohydrate, which is widely distributed in the plant kingdom. It may be composed of a single or several layers, and may possess ridges or markings of various patterns on it. In addition to the shell, gelatinous substance may in many forms be produced to surround the shelled body or in the members of Volvocidae to form the matrix of the entire colony in which the individuals are embedded. In the dinoflagellates, the shell is highly developed and often composed of numerous plates which are variously sculptured.

In other Protozoa, the shell

(tectin).

is

made up

of chitin or pseudo-chitin

Common examples are found in the testaceans; for example,

and allied forms, the shell is made up of chitinous material constructed in particular ways which characterize the different genera. Newly formed shell is colorless, but older ones become brownish,
in Arcella

form

because of the presence of iron oxide. Difflugia and related genera shells by gluing together small sand-grains, diatom-shells,

debris, etc., with chitinous or pseudochitinous substances

which

they secrete.
selective their shells.

Many

foraminiferans seem to possess a remarkable

power

in the use of foreign materials, for the construction of

According to Cushman (1933) Psammosphaera fusca uses sand-grains of uniform color but of different sizes, while P. parva uses grains of more or less uniform size but adds, as a rule, a single large acerose sponge spicule which is built into the test and which extends out both ways considerably. Cushman thinks that this is not accidental, since the specimens without the spicules are few and those with a short or broken spicules are not found. P. bowmanni, on the other hand, uses only mica flakes which are found in a comparatively small amount, and P. rustica uses acerose sponge spicules for the framework of the shell, skilfully fitting smaller broken pieces into polygonal areas. Other foraminiferans combine chitinous secretion with calcium carbonate and produce beautifully constructed shells (Fig. 4) with one or numerous pores. In the Coccolithidae, variously shaped platelets of calcium carbonate ornament the shell. The silica is present in the shells of various Protozoa. In Euglypha and related testaceans, siliceous scales or platelets are produced in the endoplasm and compose a new shell at the time of fission or of

48

PROTOZOOLOGY

encystment together with the chitinous secretion. In many heliozoans, siliceous substance forms spicules, platelets, or combination of both which are embedded in the mucilaginous envelope that surrounds the body and, in some cases, a special clathrate shell composed of
silica, is

to be found. In

some Radiolaria,

isolated siliceous

spicules occur as in Heliozoa, while in others the lateral

development

Fig. 4. Diagram of the shell of Peneroplis pertusus, X about 35 (Carpenter), ep, external pore; s, septum; sc, stolon canal.

of the spines results in production of highly

complex and the most

beautiful shells with various ornamentations or incorporation of

foreign materials.

Many

pelagic radiolarians possess

numerous con-

spicuous radiating spines in connection with the skeleton, which apparently aid the organisms in maintaining their existence in the open
sea.

lated end

Certain Protomonadina possess a funnel-like collar in the flageland in some in addition a chitinous lorica surrounds the
is

body. The lorica found in the Ciliophora

mostly composed of

chitinous substance alone, especially in Peritricha, although others

produce a house made up of gelatinous secretion containing foreign

materials as in Stentor
(p.

806).

In the Tintinnidae, the loricae

numerous marine forms not mentioned in the present work or composed of sand-grains or coccoliths cemented together by chitinous secretion, which are found in freshare either solely chitinous in

water forms.

MORPHOLOGY
Locomotor organellae

49

Closely associated with the body surface are the organellae of

locomotion: pseudopodia, flagella, and cilia. These organellae are not confined to Protozoa alone and occur in various cells of Metazoa.
All protoplasmic masses are capable of
in

movement which may result change of their forms. Pseudopodia. A pseudopodium is a temporary projection of part of the cytoplasm of those protozoans which do not possess a definite pellicle. Pseudopodia are therefore a characteristic organella of Sarcodina, though many Mastigophora and certain Sporozoa, which lack a pellicle, are also able to produce them. According to their form and structure, four kinds of pseudopodia are distinguished. 1). Lobopodium is formed by an extension of the ectoplasm, accompanied by a flow of endoplasm as is commonly found in Amoeba proteus (Figs. 46; 184). It is finger- or tongue-like, sometimes branched, and its distal end is typically rounded. It is quickly formed and equally quickly retracted. In many cases, there are many pseudopodia formed from the entire body surface, in which the largest one will counteract the smaller ones and the organism will move in one direction; while in others, there may be a single pseudopodium formed, as in Amoeba striata, A. guttula, Pelomyxa carolinensis (Fig. 186, b), etc., in which case it is a broadly tonguelike extension of the body in one direction and the progressive movement of the organisms is comparatively rapid. The lobopodia may occasionally be conical in general shape, as in Amoeba spumosa (Fig. 185, a). Although ordinarily the formation of lobopodia is by a general flow of the cytoplasm, in some it is sudden and "eruptive," as in Entamoeba blattae or Entamoeba histolytica in which the flow of the endoplasm presses against the inner zone of the ectoplasm and the accumulated pressure finally causes a break through the zone, resulting in a sudden extension of the endoplasmic flow at that point. 2). Filopodium is a more or less filamentous projection composed almost exclusively of the ectoplasm. It may sometimes be branched, but the branches do not anastomose. Many testaceans, such as Lecythium, Boderia, Plagiophrys, Pamphagus, Euglypha, etc., form this type of pseudopodia. The pseudopodia of Amoeba radiosa may be considered as approaching this type rather than the
lobopodia.
3).

Rhizopodium
(Fig. 5),

anastomosing. It

is

Elphidium

but branching and numerous Foraminifera, such as Peneroplis, etc., and in certain testaceans, such
is

also

filamentous,

found

in

50

PROTOZOOLOGY

as Lieberkuhnia,

Myxotheca, etc. The abundantly branching and anastomosing rhizopodia often produce a large network which serves almost exclusively for capturing prey.

lift, \^i
;;\v

;;:;;: ;l

I'll:

Fig.

5.

Pseudopodia of Elphidium strigilata, (Schulze from Kiihn).

X about

50

4).

Axopodium

is,

unlike the other three types, a

more

or less

semi-permanent structure and composed of axial rod and cytoplasmic envelope. Axopodia are found in many Heliozoa, such as Actinophrys, Actinosphaerium, Camptonema, Sphaerastrum, and Acan-

MORPHOLOGY
thocystis.

51

The

axial rod,

which

(Doeflein; Roskin, 1925;

is composed of a number of Rumjantzew and Wermel, 1925),

fibrils

arises

from the central body or the nucleus located in the approximate center of the body, from each of the nuclei in multinucleate forms, or from the zone between the ectoplasm and endoplasm (Fig. 6). Although semipermanent in structure, the axial rod is easily absorbed and reformed. In the genera of Heliozoa not mentioned above and in numerous radiolarians, the radiating filamentous pseudopodia are so extremely delicate that it is difficult to determine

en

.-Ite
c

kSX

w
ec

7\A\. -| '"-/
Fig.
6.

cv, contractile vacuole; ec,

Portion of Actinosphaerium eichhorni, X800 (Kiihn). ar, axial rod; ectoplasm; en, endoplasm; n, nucleus.

whether an axial rod exists in each or not, although they resemble axopodia in general appearance. There is no sharp demarcation between the four types of pseudopodia, as there are transitional pseudopodia between any two of them. For example, the pseudopodia formed by Arcella, Lesquereusia, Hyalosphaenia, etc., resemble more lobopodia than filopodia, though composed of the ectoplasm only. The pseudopodia of Actinomonas, Elaeorhanis, Clathrulina, etc., may be looked upon as
transitional

between rhizopodia and axopodia. While the pseudopodia formed by an individual are usually of characteristic form and appearance, they may show an entirely different appearance under different circumstances. According to

52

PROTOZOOLOGY

Umax amoeba changed amoeba upon addition of potassium hydroxide to the water (Fig. 7). Mast has recently shown that when Amoeba proteus or A dubia was transferred from a salt medium into pure water, the amoeba produced radiating pseudopodia, and when transferred back to a salt medium, it changed into monopodal form, which change he was inclined to attribute to the difference in the water contents of the amoeba. In some cases during and after certain internal changes, an amoeba may show conspicuous differences in
the often-quoted experiment of Verworn, a
into a radiosa
.

forms;

Form-change in a limax-amoeba (Verworn). a, b, contracted individual showing typical form; d-f, radiosa-forms, after addition of solution to the water.
Fig.
7.
c,

KOH

pseudopodia (Neresheimer). As was stated before, pseudopodia occur widely in forms which are placed under classes other than Sarcodina during a part of their life-cycle. Care, therefore, should be exercised in using
Flagella.

them for taxonomic consideration of the Protozoa. The flagellum is a filamentous extension of the cytoplasm
it

and

is

ordinarily extremely hue

difficult to recognize

distinctly in

and highly vibratile, so that life under the microscope.

it is

It is

most

clearly observed

under a darkfield or phase microscope. Lugol's

solution usually
killed.

makes it more easily visible, though the organism is In a small number of species, the flagellum can be seen in life
in

under an ordinary microscope as a long filament, as for example

MORPHOLOGY
is

53

Peranema. As a rule, the number of flagella present in an individual small, varying from one to eight and most commonly one or two; but in Hypermastigina there occur numerous flagella. A flagellum appears to be composed of two parts: an elastic axial filament or axoneme, made up of one to several fibrils and the contractile cytoplasmic sheath surrounding the axoneme (Fig. 8, a, b). In some flagella, both components extend the entire length and terminate in a bluntly rounded point, while in others the distal portion of the axoneme is apparently very thinly sheathed (Fig. 8, c).

Fig. 8. Diagrams of flagella. a, flagellum of Euglena (Butschli); b, flagellum of Trachelomonas (Plenge); c, flagella of Polytoma uvella; d,
flagella of

Monas

socialis (Vlk).

In some

flagellates, stained flagella

show numerous

lateral fibrils

Mainx, 1929; Petersen, 1929; etc.). These flagella or ciliary flagella have also been noticed by several observers in unstained organisms under darkfield micro(Fig. 8, d) (Fischer, 1894; Dellinger, 1909;

scope (Vlk, 1938; Pitelka, 1949). In recent years, the electron microscope has been used by some to observe the flagellar structure (Schmitt, Hall and Jakus, 1943; Brown, 1945; Pitelka, 1949; Chen,
all cases, the organisms were air-dried on collodion examination so that the flagella disintegrated more or less completely at the time of observation. Pitelka (1949) studied flagella of euglenoid organisms under light and electron microscopes. She found that the flagellum of Euglena

1950), but in

films for

54
gracilis,

PROTOZOOLOGY

Astasia longa and Rhabdomonas incurva, consists of an axoneme, composed of about 9 fibrils, 350-600 A in diameter, arranged in two compact, parallel bundles, and a sheath which is made up of fibrillar elements, a probably semi-fluid matrix and a limiting membrane. Under conditions always associated with death of the organism, the fibrils of the sheath fray out on one or more sides of
the flagellum into fine lateral filaments or mastigonemes.

The

electron

micrographs obtained by various investigators on supposedly one and the same flagellate present a varied appearance of the structure. Compare, for example, the micrographs of the frayed flagellum of Euglena gracilis by Brown (1945), Pitelka (1949) and Houwink
(1951).

The

anterior flagellum of

Peranema trichophorum frays out

first

into three strands during the course of disintegration as

ob-

served by Dellinger (1909) and

easily
acidified

by

several recent observers. It can be

demonstrated by treating the organism with reagents such as methyl green. Under electron microscope, Petelka noted no frayed mastigonemes in the flagellum of Peranema, while Chen (1950) observed numerous mastigonemes extending out from all
sides like a brush, except the basal portion of the flagellum.

The
that
it

electron micrographs of the flagellum of trypanosomes reveal

also consists of an axoneme and a sheath of cytoplasm. The axoneme is composed of a number of long parallel fibrils, 8 in Tnjpanosoma lewisi, each with estimated diameters of 0. 055-0. 06m (Kleinschmidt and Kinder, 1950), and up to 9 in T. evansi, with estimated diameters of 0.04-0.05^ (Kraneveld, Houwink and Keidel, 1951). The cytoplasmic sheath of the latter species was said to be
cross-striated at

about 0.05m

intervals.

No

mastigonemes occur

in

these flagella.

The frayed condition

vidual, as revealed

of a flagellum
is still

from the organism or which

which had become detached attached to a moribund indi-

by the

darkfield microscope,

may

also indicate a

phase in disintegration of the flagellum. It is reasonable to assume that different flagella may have structural differences as revealed by the electron microscope, but evidence for the occurrence of mastigonemes on an active flagellum of a normally living organism appears not to be on hand.

flagellum takes

its origin in

bedded
large

in the cytoplasm.

The blepharoplast
it

a blepharoplast of kinetosome imis a small compact

granule, but in certain parasitic flagellates,

may

be comparatively

and ovoid or short rod-shaped, surrounded often by a halo. Whether this is due to the presence of a delicate cortical structure enveloping the compact body or to desiccation or fixation is un-

MORPHOLOGY
known. In such forms, the flagellum appears to
of the halo.

55
arise

from the outer (1906), Minchin (1912), etc., used the term kinetonucleus. It has since been found that the blepharoplast of certain trypanosomes often gives a positive Feulgen's reaction (Bresslau and Scremin, 1924). The blepharoplast and centriole are considered synonymous by some, since prior to the division of nucleus, it divides and initiates the division of the latter. A new flagellum arises from one of the daughter blepharoplasts. While the blepharoplast is inseparably connected with the flagellum and its activity, it is exceedingly small or absent in Trypanosoma equinum and in some strains of T. evansi. Furthermore, this condition may be produced by exposure of normal
edge
Certain observers such as

Woodcock

individuals to certain chemical substances (Jirovec, 1929; Piekarski,

1949) or spontaneously (p. 228) without decrease in flagellar activity. The flagellum is most frequently inserted near the anterior end
of the body and directed forward, its movement pulling the organism forward. Combined with this, there may be a trailing flagellum which is directed posteriorly and serves to steer the course of movement or to push the body forward to a certain extent. In a comparatively small number of flagellates, the flagellum is inserted near the posterior end of the body and would push the body forward by its

vibration.
flagella.

terior

Under favorable conditions, flagellates regenerate lost For example, Peranema trichophorum from which its anflagellum w as cut off, regenerated a new one in two hours
r

(Chen, 1950). In certain parasitic Mastigophora, such as Trypanosoma (Fig. 9), Trichomonas, etc., there is a very delicate membrane extending out from the side of the body, a flagellum bordering its outer margin.

When

this

membrane

vibrates,

it

movement, frog, and is

as will easily be seen in

called the undulating

shows a characteristic undulating Trypanosoma rotatorium of the

membrane. In many

of the dino-

flagellates, the transverse flagellum

seems to be similarly constructed

(Kofoid and Swezy) (Fig. 127, d,f).

phora.

The cilia are the organella of locomotion found in the CilioThey aid in the ingestion of food and serve often as a tactile organella. The cilia are fine and more or less short processes of ectoCilia.

plasm and occur

in large

numbers

in the

They may be uniformly

long, as in Protociliata, or

majority of the Holotricha. may be of differ-

ent lengths, being longer at the extremities, on certain areas, in peristome or in circumoral areas. Ordinarily the cilia are arranged in
longitudinal, oblique, or spiral rows, being inserted either on the
ridges or in the furrows.

A cilium originates in a kinetosome embedded

56
in the ectoplasm.

PROTOZOOLOGY

In well-studied ciliates, there occurs a fine fibril, kinetodesma (Chatton and Lwoff, 1935), a short distance to the right
of the

kinetosome

(Fig. 23).

The

ciliary

row or kinety (Chatton and

Lwoff) consists of the kinetosomes and kinetodesma (Fig. 23, a). In forms such as Suctoria in which cilia occur only in the swimming
stage, the kinetosomes

appear to be present as infraciliature (Chat-

ton, Lwoff

and Lwoff, 1929).

Flagellum

Undulating

membrane

Nucl(

Blepharoplast

Fig.

9.

diagram showing the structure

of a

trypanosome (Ktihn).

As

to its structure, a cilium appears to be

(Fig. 10, a). Gelei

made up

of

an axoneme

and contractile sheath

observed in flagella and cilia, lipoid substance in granular or rod-like forms which differed even among different individuals of the same species; and Klein
(1929) found in

many

cilia of

substance in granular form

Gelei and called
(Fig. 10,
b, c).

much

Colpidium colpoda, an argentophilous resembling the lipoid structure of

them "cross

striation" of the contractile

component

In electron micrographs of a dried cilium of Paramecium, Jakus and Hall (1946) found that it consisted of a bundle of about 11 fibrils extending the full length (Fig. 10, d). These fibrils

were about 300-500

fragile

in diameter.
if

As

there

was no

visible sheath,

the two observers remarked that

a sheath exists,

it

must be very

and
cilia

easily ruptured.

in other parts of

more densely in a certain area than body and, consequently, such an area stands out conspicuously, and is sometimes referred to as a ciliary field. If this area is in the form of a zone, it may be called a ciliary zone. Some
are often present

The

authors use pectinellae for short longitudinal rows or transverse

MORPHOLOGY
bands
of close-set cilia. In a
tor, etc., there occur,
stiff cilia

57

number of forms, such as Coleps, Stenmingled among the vibratile cilia, immobile which are apparently solely tactile in function.

Fig. 10. a, cilia of Coleps; b, cilium of Cyclidium glaucoma; c, basal portion of a cilium of Colpidium colpoda, all in silver preparations (Klein); d, electronmicrograph of a dried cilium of Paramecium, shadow-cast with

chromium, XI 1,000 (Jakus and Hall).

In the Hypotricha, the
in
cilia

are largely replaced

by

cirri,

although

some

species both

may

occur.

A cirrus is composed of a number of

cilia

pletely (Figs. 11, a; 12, a),

arranged in 2 to 3 rows that fused into one structure comwhich was demonstrated by Taylor. Klein also showed by desiccation that each marginal cirrus of Stylonychia

58

PROTOZOOLOGY

was composed of 7 to 8 cilia. In some instances, the distal portion of a may show two or more branches. The cirri are confined to the ventral surface in Hypotricha, and called frontal, ventral, anal,
cirrus

Cirrus fiber

Ectoplasmic granules
Basal plate of the cirrus

Kinetosomes

of
cilia

component

Adoral zone
Frontal
cirri

Undulating membrane

Marginal
Ventral

cirri

cirri

Anal

cirri

Caudal

cirri

Fig. 11. a, five anal cirri of Euplotes eurystomus (Taylo'r); b, schematic ventral view of Stylonychia to show the distribution of the cirri.

cirri, according to their location (Fig. 11, b). Unlike cilia, the cirri may move in any direction so that the organisms bearing them show various types of locomotion. Oxytricha,

caudal, and marginal

MORPHOLOGY
Stylonychia,

59

etc., "walk" on frontals, ventrals, and anals, while swimming movement by other species is of different types.

In

all euciliates

membranella

is

except Holotricha, there are adoral membranellae. composed of a double ciliary lamella, fused com-

pletely into a plate (Fig. 12, b).

A number

of these

membranellae

occur on a margin of the peristome, forming the adoral zone of

cpg

Fig. 12. Diagrams of cirrus and membranella of Euplotes eurystomus, (Taylor), a, anal cirrus in side view; b, a membranella (cpg, coagulated protoplasmic granules; cr, ciliary root; fp, fiber plate; k, kineto-

X1450

some)

membranellae, which serves for bringing the food particles to the cytostome as well as for locomotion. The frontal portion of the zone, the so-called frontal membrane appears to serve for locomotion and Kahl considers that it is probably made up of three lamellae. The oral membranes which are often found in Holotricha and Heterotricha, are transparent thin membranous structures composed of one or two
of cilia, which are more or less strongly fused. The membranes, located in the lower end of the peristome, are sometimes called

rows

perioral

membranes, and those

cilia

in the cytopharynx, undulating

mem-

branes.
stages, and, as the

are present only during the developmental organisms become mature, tentacles develop in their stead. The tentacles are concerned with food-capturing, and

In Suctoria,

60

PROTOZOOLOGY

are either prehensile or usually suctorial. The prehensile tentacle appears to be essentially similar in structure to the axopodium

(Roskin, 1925).
interpreted

The

suctorial tentacles are tubular

and

this

type

is

by

Collin as possibly derived from cytostome and cyto-

pharynx of the ciliate (Fig. 13). Although the vast majority of Protozoa possess only one of the three organelles of locomotion mentioned above, a few may possess

jjjgjt

Fig. 13.

tentacle from a cytostome

Diagrams showing the possible development of a suctorian and cytopharynx of a ciliate (Collin).

pseudopodia in one stage and flagella in another during their development. Among several examples may be mentioned Naegleriidae (Fig. 183), Tetramitus rostratus (Fig. 155), etc. Furthermore, there are some Protozoa which possess two types of organellae at the same time. Flagellum or flagella and pseudopodia occur in many Phytomastigina and Rhizomastigina, and a flagellum and cilia are
present in Ileonema (Fig. 306,
b, c).

In the cytoplasm of Protozoa there occur various organellae, each of which will be considered here briefly.
Fibrillar structures

fundamental characteristics of the protoplasm is its contractility. If a fully expanded Amoeba proteus is subjected to a mechanical pressure, it retracts its pseudopodia and contracts into a more or less spherical form. In this response there is no special organella, and the whole body reacts. But in certain other Protozoa,
of the

One

there are special organellae of contraction.

to contract instantaneously as will easily

Many

Ciliophora are able

when subjected to mechanical pressure, be noticed by following the movement of Stentor,

etc.,

Spirostomum, Trachelocerca, Vorticella,

microscope.

under a dissecting

elements of Protozoa appears to be Lieberkiihn (1857) who noted the "muscle

earliest observer of the contractile

The

MORPHOLOGY
fibers"
in

61

the ectoplasm of

Stentor

which were later named

several in-

myonemes (Haeckel) or neurophanes (Neresheimer). The myonemes of Stentor have been studied by
vestigators. According to Schroder (1906), there
is

a canal between

each two longitudinal striae and in it occurs a long banded myoneme which measures in cross-section 3-7/x high by about lju wide and which appears cross-striated (Fig. 14). Roskin (1923) considers that

mc

gis

Fig. 14. Myonemes in Stentor coeruleus (Schroder), a, cross-section of the ectoplasm; b, surface view of three myonemes; c, two isolated myonemes (cl, cilium; gis, granules between striae; k, kinetosome; m,

myoneme; mc, myoneme

the

canal).

of the canal

a homogeneous cytoplasm (kinoplasm) and the wall highly elastic and counteracts the contraction of the myonemes. All observers agree that the myoneme is a highly con-

myoneme

is

is

tractile organella.

Many stalked peritrichous

ciliates

have well-developed myonemes

not only in the body proper, but also in the stalk. Koltzoff's (1911) studies show that the stalk is a pseudochitinous tube, enclosing an inner tube filled with granulated thecoplasm, which surrounds a central rod,

composed

of

kinoplasm, on the surface of which are ar-

62

PROTOZOOLOGY

ranged skeletal fibrils (Fig. 15). The contraction of the stalk is brought about by the action of kinoplasm and walls, while elastic

Myonemes present in the body, but those which occur in many Gregarinida aid apparently in locomotion, being arranged longitudinally, transversely and probably spirally (Roskin and Levinsohn, 1929) (Fig. 15, c). In certain Radiolaria, such as Acanthorods will lead to extension of the stalk.
ciliates aid in the contraction of

zoff); c,

Fig. 15. a, b, fibrillar structures of the stalk of Zoothamnium (Koltmyonemes in Gregarina (Schneider), ef, elastic fiber; ie, inner
t,

envelope; k, kinoplasm; oe, outer envelope;

thecoplasm.

metron elasticum (Fig. 219, c), etc., each axial spine is connected with 10-30 myonemes (myophrisks) originating in the body surface.

When

these

myonemes

contract, the

body volume

is

increased, thus

in this case functioning as a hydrostatic organella.

/. intestinalis, Schuberg (1888) observed suspended by ectoplasmic fibrils and called the apparatus karyophore. In some forms these fibrils are replaced by ectoplasmic membranes as in Nyctotherus ovalis (Zulueta; Kudo), ten Kate (1927, 1928) studied fibrillar systems in Opalina, Nycto-

In Isotricha prostoma and

is

that the nucleus

MORPHOLOCxY
therus, Ichthyophthirius, Didinium,

63

that there are numerous

fibrils,

and Balantidium, and found each of which originates in the kine-

tosome of a cilium and takes a transverse or oblique course through the endoplasm, ending in a kinetosome located on the other side of the body. He further noted that the cytopharynx and nucleus are also connected with these fibrils, ten Kate suggested morphonemes for them, since he believed that the majority were form-retaining
fibrils.

The well-coordinated movement

been recognized, but
it

of cilia in the ciliate has long

was Sharp (1914) who definitely showed that this ciliary coordination is made possible by a certain fibrillar system which he discovered in Epidinium (Diplodinium) ecaudatum (Fig. 16). Sharp recognized in this ciliate a complicated fibrillar system connecting all the motor organellae of the cytostomal region, and thinking that it was "probably nervous in function," as its size, arrangement and location did not suggest supporting or contractile function, he gave the name neuromotor apparatus to the whole system. This apparatus consists of a central motor mass, the motorium (which is stained red with Zenker fixation and modified
Mallory's connective tissue staining), located in the ectoplasm just above the base of the left skeletal area, from which definite strands radiate: namely, one to the roots of the dorsal membranellae (a dorsal motor strand) one to the roots of the adoral membranellae (a ventral motor strand); one to the cytopharynx (a circum-oesophageal ring and oesophageal fibers) and several strands into the ectoplasm of the operculum (opercular fibers). A similar apparatus has since been observed in many other ciliates: Euplotes (Yocom; Taylor), Balantiduum (McDonald), Paramecium (Rees; Brown; Lund), Tintinnopsis (Campbell), Boveria (Pickard), Dileptus (Visscher), Chlamydodon (MacDougall), Entorhipidium and Lechriopyla (Lynch), Eupoterion (MacLennan and Connell), Metopus (Lucas), Troglodytella (Swezey), Oxytricha (Lund), Ancistruma and Conchophthirus (Kidder), etc. Ciliate fibrillar systems (Taylor,
; ;

1941).

Euplotes, a

common

free-living hypotrichous ciliate, has

been

known
anal

for nearly 60 years to possess definite fibrils connecting the

cirri

with the anterior part of the body. Engelmann suggested

that their function was more or less nervelike, while others maintained that they were supporting or contracting in function. Yocom
(1918) traced the fibrils to the motorium, a very small bilobed

body
five

(about

8/x

by

2ju)

located close to the right anterior corner of the

its left

triangular cytostome (Fig. 17, m). Joining with

end are

composite drawing from three median sagittal sections of fixed in Zenker and stained with Mallory's connective tissue stain, X1200 (Sharp), am, adoral membranellae; c, cytostome; cp, cytopharynx; cpg, cytopyge; cpr, circumpharyngeal ring; dd, dorsal disk; dm, dorsal membrane; ec, ectoplasm; en, endoplasm; m, motorium; oc, oral cilia; od, oral disk; oef, oesophageal fibers; of, opercular fibers; p, pellicle; prs, pharyngeal retractor strands; si, skeletal laminae; vs, venFig. 16.

Epidinium ecaudatum,

tral skeletal area.

MORPHOLOGY

65

long fibers (acf) from the anal cirri which converge and appear to unite with the motorium as a single strand. From the right end of the

motorium extends the membranella-fiber anteriorly and then to

left

along the proximal border of the oral lip and the bases of all membranellae. Yocom further noticed that within the lip there is a

sm

Fig. 17. Ventral view of Euplotes eurystomus (E. patella) showing neuromotor system, X670 (Hammond), acf, fibril of anal cirrus; am, anterior adoral zone membranelle; m, motorium; mf, membranelle fibrils; oc, en-

doral cilia; pf, post-pharyngeal fibril; pra, post-pharyngeal membrane; rf, radiating fibrils; sm, suboral membranelles; vm, ventral adoral zone

membranelles.

latticework structure whose bases very closely approximate the cyto-

stomal

fiber.

fibrils in

Taylor (1920) recognized two additional groups of the same organism: (1) membranella fiber plates, each of
is

which

is

contiguous with a membranella basal plate, and

attached
con-

at one end to the

membranella

fiber; (2) dissociated fiber plates

tiguous with the basal plates of the frontal, ventral and marginal
cirri,

to each of which are attached the dissociated fibers

of microdissection needles,

(rf).

By

means

Taylor demonstrated that these

66
fibers

PROTOZOOLOGY

since there results

have nothing to do with the maintenance of the body form, no deformity when Euplotes is cut fully twothirds its width, thus cutting the fibers, and that when the motorium is destroyed or its attached fibers are cut, there is no coordination in the movements of the adoral membranellae and anal cirri. Hammond (1937) and Hammond and Kofoid (1937) find the neuromotor system continuous throughout the stages during asexual reproduction and conjugation so that functional activity is maintained at all
times.

striking feature

there seems to be a central

different ciliary

to all neuromotor systems, is that motorium from which radiate fibers to structures and that, at the bases of such motor or-

common

ganellae, are

found the kinetosomes or basal plates to which the

"nerve" fibers from the motorium are attached. Independent of the studies on the neuromotor system of American investigators, Klein (1926) introduced the silver-impregnation method which had first been used by Golgi in 1873 to demonstrate various fibrillar structures of metazoan cells, to Protozoa in order
to demonstrate the cortical fibers present in ciliates,

by

dry-fixation

and impregnating with silver nitrate. Klein (1926-1942) subjected ciliates of numerous genera and species to this method, and observed that there was a fibrillar system in the ectoplasm at the level of the kinetosomes which could not be demonstrated by other methods. Klein (1927) named the fibers silver lines and the whole complex, the silverline system, which vary among different species (Figs. 1820). Gelei, Chatton and Lwoff, Jlrovec, Lynch, Jacobson, Kidder. Lund, Burt, and others, applied the silver-impregnation method to many other ciliates and confirmed Klein's observations. Chatton and Lwoff (1935) found in Apostomea, the system remains even after the embryonic cilia have entirely disappeared and considered it infraciliature.

the neuromotor apparatus and the silversystem are independent structures or different aspects of the same structure has been raised frequently. Turner (1933) found that in Euplotes patella (E. eurystomus) the silverline system is a regular latticework on the dorsal surface and a more irregular network on the ventral surface. These lines are associated with rows of rosettes from which bristles extend. These bristles are held to be sensory in function and the network, a sensory conductor system, which is connected with the neuromotor system. Turner maintains that the neuromotor apparatus in Euplotes is augmented by a distinct but connected external network of sensory fibrils. He however finds no

The question whether

line

motorium

in this protozoan.

MORPHOLOGY
in

(17

Lund (1933) also made a comparative study of the two systems Paramecium multimicronucleatum, and observed that the silverline system of this ciliate consists of two parts. One portion is made up
of a series of closely-set polygons, usually hexagons,

but flattened

into rhomboids or other quadrilaterals in the regions of the cytostome, cytopyge, and suture. This system of lines stains if the or-

Fig. 18.

The

silverline
a,

system

of

Ancistruma

mytili,

XlOOO (Kidder).

ventral view; b, dorsal view.

ganisms are well dried. Usually the lines appear solid, but frequently they are interrupted to appear double at the vertices of the polygons which Klein called "indirectly connected" (pellicular) conductile system. In the middle of the anterior and posterior sides of the hexagons is found one granule or a cluster of 2-4 granules, which marks the outer end of the trichocyst. The second part which Klein called "directly connected" (subpellicular) conductile system
consists essentially of the longitudinal lines connecting all kine-

tosomes in a longitudinal row of hexagons and of delicate transverse fibrils connecting granules of adjacent rows especially in the cytostomal region (Fig. 19). By using Sharp's technique, Lund found the neuromotor system

68
of

PROTOZOOLOGY
Paramecium multimicronucleatum constructed
is

as follows:
fibrils

The

subpellicular portion of the system

the longitudinal

which

connect the kinetosomes. In the cytostomal region, the fibrils of right and left sides curve inward forming complete circuits (the circular cytostomal fibrils) (Fig. 20). The postoral suture is separated at the point where the cytopyge is situated. Usually 40-50 fibrils

Fig. 19. Diagram of the cortical region of Paramecium multimicronucleatum, showing various organellae (Lund), c, cilia; et, tip of trichocyst; k, kinetosome; If, longitudinal fibril; p, pellicle; t, trichocyst; tf, transverse
fibril.

radiate outward from the cytostome (the radial cytostomal

fibrils).

more complex and consists of (1) the oesophageal network, (2) the motorium and associated fibrils, (3) penniculus which is composed of 8 rows of kinetosomes, thus forming a heavy band of cilia in the cytopharynx, (4) oesophageal process, (5) paraoesophageal fibrils, (6) posterior neuromotor chain, and (7)

The pharyngeal portion

is

postoesophageal

fibrils.

Lund

concludes that the so-called silverline

system includes three structures: namely, the peculiarly ridged pellicle; trichocysts which have no fibrillar connections among them or with fibrils, hence not conductile; and the subpellicular system, the last of which is that part of the neuromotor system that concerns with the body cilia, ten Kate (1927) suggested that sensomotor apparatus is a better term than the neuromotor apparatus.
Silverline

system (Klein, 1926-1942; Gelei, 1932);

fibrils in ciliates

Fig. 20.

The neuromotor system

oral network; b,

of

Paramecium multimicronucleahim

motorium, X1670. aep, anterior end of penniculus; c, cytopyge; ccf, circular cytostomal fibril; cof, circular oesophageal fibril; cpf, circular pharyngeal fibril; ef, endoplasmic fibrils; lbf,
(Lund),
a,

longitudinal body fibril; lof, longitudinal oesophageal fibrils; lpf, longitudinal pharyngeal fibril; m, motorium; oo, opening of oesophagus; op, oesophageal process; paf, paraoesophageal fibrils; pep, posterior end of penniculus; pnc, posterior neuromotor chain; pof, postoesophageal fibrils; rcf, radial cytostomal fibril; s, suture.

70

PROTOZOOLOGY

(Jacobson, 1932; Taylor, 1941); argyrome in Astomata (Puytorac,

1951).

Protective or supportive organ ellae

The

external structures as found

among

various Protozoa which

serve for

body

protection, have already been considered (p. 47).

will be discussed. The greater part Foraminifera is to be looked upon as endoskeleton and thus supportive in function. In Radiolaria, there is a membranous structure, the central capsule, which divides the body into

Here certain internal structures

of the shell of

a central region and a peripheral zone. The intracapsular portion contains the nucleus or nuclei, and is the seat of reproductive processes,

and thus the capsule

is

to be considered as a protective or-

ganella.

The

position
(p.

vary in chemical comand forms, and are arranged with a remarkable regularity
skeletal structures of Radiolaria

517).

In some of the astomatous euciliates, there are certain structures which seem to serve for attaching the body to the host's organ, but

which seem to be supportive to a certain extent

organella furcula, observed

also.

The

peculiar
is

by Lynch

in Lechriopyla (p. 741)

said

neuromotor system or protection. The members of the family Ophryoscolecidae (p. 816), which are common commensals in the stomach of ruminants, have conspicuous endoskeletal plates which arise in the oral region and extend posteriorly. Dogiel (1923) believed that the skeletal plates of Cycloposthium and Ophryoscolecidae are made up of hemicellulose, "ophryoscolecin," which was also observed by Strelkow (1929). MacLennan found that the skeletal plates of Polyplastron multivesiculatum were composed of small, roughly prismatic blocks of paraglycogen, each
to be concerned with either the

possessing a central granule.

flexible structure

In certain Polymastigina and Hypermastigina, there occurs a known as the axostyle, which varies from a filamentous structure as in several Trichomonas, to a very conspicuous

Gigantomonas, etc. The very close to the anterior tip of the body, and it extends lengthwise through the cytoplasm, ending near the posterior end or extending beyond the body surface. In other cases, the axostyle is replaced by a bundle of axostylar filaments that are connected with the flagella (Lophomonas). The axostyle appears to be supportive in function, but in forms such as Saccinobaculus, it undulates and aids in locomotion (p. 379). In trichomonad flagellates there is often present along the line of
rod-like structure occurring in Parajoenia,

anterior end of the axostyle

is

"

MORPHOLOGY

71

attachment of the undulating membrane, a rod-like structure which has been known as costa (Kunstler) and which, according to Kirby's extensive study, appears to be most highly developed in Pseudotrypanosoma and Trichomonas. The staining reaction indicates that its chemical composition is different from that of flagella, blepharoplast, parabasal body, or chromatin. In the gymnostomatous ciliates, the cytopharynx is often surrounded by rod-like bodies, and the entire apparatus is often called oral or pharyngeal basket, which is considered as supportive in function. These rods are arranged to form the wall of the cytopharynx in a characteristic way. For example, the oral basket of

which are so completely fused

of 12 long rods appears to be a smooth tube; in other forms, the rods are evidently similar to the tubular

Chilodonella cucullulus (Fig. 312,

c,

d)

is

made up
it

in part that

trichocysts or trichites mentioned below.

In numerous holotrichs, there occur unique organelles, trichocysts, imbedded in the ectoplasm, and usually arranged at right angles to the body surface, though in forms such as Cyclogramma, they are arranged obliquely. Under certain stimulations, the trichocysts "explode" and form long filaments which extend out into the surrounding medium. The shape of the trichocyst varies somewhat among
different ciliates,, being pyriform, fusiform or cylindrical (Penard,

1922; Kriiger, 1936).

They appear
is

as

homogeneous

refractile bodies.

The extrusion

of the trichocyst

easily

brought about by means

of

mechanical pressure or of chemical (acid or alkaline) stimulation. In forms such as Paramecium, Frontonia, etc., the trichocyst is elongate pyriform or fusiform. It is supposed that within an expansible
for the
is a layer of swelling body which is responsible remarkable longitudinal extension of the membrane (Kriiger) (Fig. 21, a). In other forms such as Prorodon, Didinium, etc., the tubular trichocyst or trichites are cylindrical in shape and the membrane is a thick capsule with a coiled thread, and when stimulated, the extrusion of the thread takes place. The trichites of Prorodon

membrane, there

measure about 101 1 long (Fig. 21, d) and when extruded, the whole measures about 20 /x; those of Didinium nasutum are 1520m long and after extrusion, measure about 40 m in length (Fig. 21,
teres
yu.

e,f).

In Spathidium spathida (Fig. 21,

c),

trichites are

imbedded

like

a paling in the thickened rim of the anterior end.

They

are also

distributed throughout the endoplasm and, according to Woodruff

and Spencer, "some

of these are

transported to the oral region, while others

apparently newly formed and beingmay well be trichites

of

which have been torn away during the process

prey ingestion,

72

PROTOZOOLOGY

datum (Kruger)

a schematic drawing of the trichocyst of Paramecium cau(b, base of the tip; c, cap; m, membrane; mt, membrane of extruded trichocyst; s, swelling body; t, tip); b, an extruded trichocyst, viewed under phase dark contrast, X1800; c, trichites in Spathidium, spathula, X300 (Woodruff and Spencer); d, a diagram of the trichocyst of Prorodon teres (Kruger) (eg, capsule-granule; e, end-piece of filament; f, filament; w, capsule wall); e, f, normal and extruded trichocysts of Didinium nasutum (Kruger).
Fig. 21.
a,

MORPHOLOGY

73

Whether the numerous 12-20^ long needle-like structures which Kahl observed in Remanella (p. 727) are modified trichites or not, is not known.
Dileptus anser feeds on various ciliates through the cytostome,

band of long organisms come in contact with the ventral side of the proboscis, they give a violent jerk, and remain motionless. Visscher saw no formed elements discharged from the trichocysts, and, therefore, considered that these trichotrichocysts on
its

located at the base of the proboscis, which possesses a

ventral side.

When food

and named them toxicysts. But Kruger and Hayes (1938) found that the extruded trichocysts can be recogcysts contained a toxic fluid
nized.

Perhaps the most frequently studied trichocysts are those of Paramecium. They are elongate pyriform, with a fine tip at the broad end facing the body surface. The tip is connected with the pellicle (Fig. 19, 0- Kruger found this tip is covered by a cap (Fig. 21, a) which can be seen under darkfield or phase microscope and which was demonstrated by Jakus (1945) in an electron micrograph
(Fig. 22, a). When extruded violently, the entire structure is to be found outside the body of Paramecium. The extruded trichocyst is

composed

of

two

parts: the tip

tip is a small inverted tack,

and the main body (Fig. 21, b). The and may be straight, curved or bent.
tip.

The main body

or shaft

is

a straight rod, tapering gradually into a

sharp point at the end opposite the

Extruded trichocysts meas-

ure 20-40yu or more in length, and do not show any visible struc-

base of the tuck-shaped tip (Fig. 21, b). The electron microscope studies of the extruded trichocysts by Jakus (1945), Jakus and Hall (1946) and Wohlfarth-Bottermann (1950), show the shaft to be cross-striated

tures, except a highly refractile granule present at the

Jakus considers that the main component of the trichomembrane formed by close packing of longitudinal fibrils characterized by a periodic pattern (somewhat resembling that of collagen), and as the fibrils are in phase with re(Fig. 22).
is

cyst

a thin cylindrical

spect to this pattern, the

membrane appears

cross-striated.
is

As

to the

mechanism

of the extrusion,

no precise information

though all observers agree that the contents of the trichocyst suddenly increase in volume. Kruger maintains that the trichocyst cap is first lifted and the swelling body increases enormously in volume by absorbing water and lengthwise extension takes place, while Jakus is inclined to think that the membrane itself extends by the sudden uptake of water.
available,

74

PROTOZOOLOGY

How

are these organelles formed? Tonniges (1914) believes that

the trichocysts of Frontonia leucas originate in the endosomes of the

macronucleus and development takes place during their migration

Brodsky (1924) holds that the trichocyst is composed of colloidal excretory substances and is first formed in the vicinity of the macronucleus. Chatton and Lwoff (1935) find howto the ectoplasm.

Fig. 22. Electronmicrographs of extruded trichocysts of Paramecium, dried and stained with phosphotungstic acid, XI 1,000 (Jakus); b, a similarly treated one, X 15,000 (Jakus); c, shadow-cast with chromium,
a,

X 16,000

(Jakus and Hall).

ever in Gymnodinioides the trichocysts are formed only in tomite

stage and each trichocyst arises from a trichocystosome, a granule formed by division of a kinetosome (Fig. 23, a-c). In Polyspira, the trichocyst formation is not confined to one phase, each kinetosome is said to give rise to two granules, one of which may detach itself, migrate into other part of the body and develops into a trichocyst (d). In Foettingeria, the kinetosomes divide in young trophont stage into irichitosomes which develop into trichites (e). The two authors note that normally cilia-producing kinetosomes may give rise to

MORPHOLOGY

::

trichocysts or trichites, depending upon their position (or environment) and the phase of development of the organism. Although the trichocyst was first discovered by Ellis (1769) and so named by Allman (1855), nothing concrete is yet known as to their function. Ordinarily the trichocysts are considered as a defensive organella as in the case of the oft-quoted example

Parame-

cium, but, as
ciliate

viscid

Mast demonstrated, the extruded trichocysts of this do not have any effect upon Didinium other than forming a mass about the former to hamper the latter. On the other

oides (a-c)

Fig. 23. Diagrams showing the formation of trichocysts in Gymnodiniand in Polyspira (d) and of trichites in Foettingeria (e) (Chatton and Lwoff). a, a ciliary row, composed of kinetosomes, large satellite corpuscles and kinetodesma (a solid line); b, each kinetosome divides into

two, producing trichocystosome; c, transformation of trichocystosomes into trichocysts; d, formation of trichocyst from one of the two division products of kinetosome; e, formation of trichites from the division products of kinetosomes.

hand, the trichocysts and trichites are clearly an offensive organelle in capturing food organisms in organisms such as Dileptus, Didinium, Spathidium, etc. Saunders (1925) considered that the extruded trichocysts of Paramecium serve for attachment of the body to other objects. But Wohlfarth-Bottermann (1950) saw Paramecium cauda-

tum extruding up to 300 trichocysts without any apparent external

stimulation and trichocyst-less individuals were able to adhere to
foreign objects. This worker suggested that the trichocyst secretes

calcium salt and probably also sodium and potassium, and thus may serve an osmoregulatory function. Some years ago Penard (1922) considered that some trichocysts may be secretory organellae to pro-

duce material for loricae or envelope, with which view Kahl concurs, as granular to rod-shaped trichocysts occur in Metopus, Amphilep-

76
tus, etc.

PROTOZOOLOGY
in

Klein has called these ectoplasmic granules protrichocysts, Prorodon, Kruger observed, besides typical tubular trichocysts, torpedo-like forms to which he applied the same name. To this group may belong the trichocysts recognized by Kidder in Conchophthirus mytili. The trichocysts present in certain Cryptomonadina (Chilomonas and Cyathomonas) are probably homologous with

and

the protrichocysts (Kruger, 1934; Hollande, 1942; Dragesco, 1951).

Hold-fast organellae
In the Mastigophora, Ciliophora, and a few Sarcodina, there
are forms which possess a stalk supporting the

body

or the lorica.

attached to a solid surface. In some cases, as in Ahthophysis, Maryna, etc., the dendritic stalks are made up of gelatinous substances rich in iron, which gives to them a

With the

stalk the organism

is

reddish brown color. In parasitic Protozoa, there are special organellae developed for attachment.
(Figs. 235-237),

Many

genera

of

cephaline

gregarines are provided with an epimerite of different structures

by which the organisms are able to attach themetc.,

selves to the gut epithelium of the host. In Astomata, such as Intoshellina,

Maupasella, Lachmannella,

simple or complex profor ad-

trusible chitinous structures are often present in the anterior region

or a certain area of the

body may be concave and serves

hesion to the host, as in Rhizocaryum, Perezella, etc.; or, again, there may be a distinctive sucker-like organella near the anterior

extremity of the body, as in Haptophyra, Steinella, etc. A sucker is also present on the antero-ventral part of Giardia intestinalis. In the Myxosporidia and Actinomyxidia, there appear, during the development of spore, 1-4 special cells which develop into polar capsules, each, when fully formed, enclosing a more or less
long spirally coiled delicate thread, the polar filament (Figs. 279, 286). The polar filament is considered as a temporary anchoring orits germination after it gained entrance into the alimentary canal of a suitable host. In the Microsporidia, the filament may or may not be enclosed within a capsule (Figs. 288; 289). The nematocysts (Fig. 132, b) of certain dino-

ganella of the spore at the time of

belonging to Nematoidium and Polykrikos, are almost found in the coelenterates. They are distributed through the cytoplasm, and various developmental stages were noticed by Chatton, and Kofoid and Swezy, which indiflagellates

identical in structure with those

cates that they are characteristic structures of these dinoflagellates

and not foreign

in origin as

had been held by some. The function

is

of

the nematocysts in these protozoans

not understood.

MORPHOLOGY
Parabasal apparatus
In the cytoplasm of

77

many

parasitic flagellates, there

is

frequently

present a conspicuous structure

(Cleveland), which latter

known

as the parabasal apparatus

body and often thread be absent in some cases. This structure varies greatly among different genera and species in appearance, structure and position within the body. It is usually connected with
(Janicki, 1911), consisting of the parabasal

may

Fig. 24. Parabasal apparatus in: a, Lophomonas blattarujn (Kudo); Metadevescovina debilis; c, Devescovina sp. (Kirby). af, axostylar filaments; bl, blepharoplasts; f, food particles; fl, flagella; n, nucleus; pa, parabasal apparatus.
b,

the blepharoplast

and located very

it.

close to the nucleus,

though

not directly connected with

be single, double, or multiple, and may be pyriform, straight or curved rod-like, bandform, spirally coiled or collar-like (Fig. 24). Kofoid and Swezy considered that the parabasal body is derived from the nuclear chromatin, varies in size according to the metabolic demands of the organism, and is a
It

may

"kinetic reservoir." On the other hand, Duboscq and Grasse" (1933) maintain that this body is the Golgi apparatus, since (1) acetic acid destroys both the parabasal body and the Golgi apparatus (2) both are demonstrable with the same technique; (3) the parabasal body
;

78
is

PROTOZOOLOGY
made up
of

chromophile and chromophobe parts as is the Golgi (4) there is a strong evidence that the parabasal body is secretory in function. According to Kirby (1931), who has made an extensive study of this organella, the parabasal body could be stained with Delafield's haematoxylin or Mallory's triple stain after fixation with acetic acid-containing fixatives and the body does not show any evidence to indicate that it is a secretory organella. Moreover the parabasal body is discarded or absorbed at the time of division of the body and two new ones are formed.
apparatus; and

The parabasal body

triole or

of

Lophomonas blattarum

is

discarded

when

the organism divides and two

portive. Possibly not

new ones

are reformed from the cen-

blepharoplast (Fig. 65), and its function appears to be supall so-called parabasal bodies are homologous

or analogous.

A fuller

of the organella rests

comprehension of the structure and function on further investigations.

Golgi apparatus

With the discovery of a wide distribution of the so-called Golgi apparatus in metazoan cells, a number of protozoologists also reported a homologous structure from many protozoans. It seems impossible at present to indicate just exactly what the Golgi apparatus is, since the so-called Golgi techniques, the important ones of

which are based upon the assumption that the Golgi material is osmiophile and argentophile, and possesses a strong affinity to neutral red, are not specific and the results obtained by using the same method often vary a great deal. Some of the examples of the Golgi apparatus reported from Protozoa are summarized in Table 2. It appears thus that the Golgi bodies occurring in Protozoa are small osmiophilic granules or larger spherules which are composed of osmiophile cortical and osmiophobe central substances. Frequently the cortical layer is of unequal thickness, and, therefore, crescentic forms appear. Ringform apparatus was noted in Chilodonella and Dogielella by Nassonov (1925) and network-like forms were observed by Brown in Pyrsonympha and Dinenympha. The Golgi apparatus of Protozoa as well as of Metazoa appears to be composed of a lipoidal material in combination with protein substance.

In line with the suggestion made for the metazoan cell, the Golgi apparatus of Protozoa is considered as having something to do with
secretion or excretion.
lipoidal substance,

Nassonov (1924) considers that osmiophilic

which he observed in the vicinity of the walls of the contractile vacuole and its collecting canals in many ciliates and


MORPHOLOGY
Table
Protozoa
2.

79

Golgi apparatus in Protozoa

80

PROTOZOOLOGY

zoa (Hall, 1931; Hall and Nigrelli, 1937). The exact morphological and physiological significance of these organellae and the relation between them must be looked for in future investigations. Golgi apparatus in Protozoa (Alexeieff, 1928; MacLennan, 1941; Grasse\
1952).

Chondriosomes
Widely distributed in many metazoan cells, the chondriosomes have also been recognized in various Protozoa. The chondriosomes possess a low refractive index, and are composed of substances easily

IIS

Fig. 25.

The Golgi bodies

in

Amoeba

proteus (Brown).

soluble in alcohol, acetic acid, etc.

Osmium
:

tetroxide blackens the

chondriosomes, but the color bleaches faster than in the Golgi bodies. Janus green B stains them even in 1 500,000 solution, but stains also other inclusions, such as the Golgi bodies (in some cases) and certain bacteria. According to Horning (1926), janus red is said to be a more
exclusive chondriosome stain, as
it does not stain bacteria. The chemical composition of the chondriosome seems to be somewhat similar to that of the Golgi body; namely, it is a protein compounded with a lipoidal substance. If the protein is small in amount, it is said to be unstable and easily attacked by reagents; on the other

hand,

if

the protein

is

relatively abundant,

it is

more

stable

and

resistant to reagents.

The chondriosomes occur

as small spherical to oval granules, rod-

MORPHOLOGY
like or

81

filamentous bodies, and show a tendency to adhere to or re-

main near protoplasmic surfaces. In many cases they are distributed without any definite order; in others, as in Paramecium or Opalina, they are regularly arranged between the kinetosomes of cilia (Horning). In Tillina canalifera, Turner (1940) noticed that the endoplasmic chondriosomes are evenly distributed throughout the cytoplasm (Fig. 26, b), while the ectoplasmic chondriosomes are ar-

Sic.

<x
}

v r

m^'

Fig. 26. Chondriosomes in Tillina canalifera (Turner), a, diagram showing the ectoplasmic chondriosomes (c, cilium; cf, coordinating fibril; ch, chondriosome; cr, ciliary rootlet; k, kinetosome I and II; p, pellicle); b, a
section showing chondriosomes

and food vacuoles.

ranged in regular cross rows, one in the center of each square formed by four cilia (Fig. 2f6, a). In Peranema trichophorum, Hall (1929) observed peripheral chondriosomes located along the spiral striae, which Chadefaud (1938) considered as mucus bodies. Weisz (1949,
1950) finds that stentorin and zoopurpurin already mentioned (p.
45) are chondriosomes.
strable.

In certain Protozoa, the chondriosomes are not always demonFor example, Horning states in Monocystis the chondrio-

somes present throughout the asexual life-cycle as rod-shaped bodies, but at the beginning of the spore formation they decrease in size and number, and in the spore none exists. The chondriosomes appear as soon as the sporozoites are set free. Thus it would appear that the

82

PROTOZOOLOGY

chondriosomes are reformed de novo. On the other hand, FaureFremiet, the first student of the chondriosomes in Protozoa, maintained that they reproduce by division, which has since been confirmed by many observers. As a matter of fact, Horning found in Opalina, the chondriosomes are twisted filamentous structures and undergo multiple longitudinal fission in asexual division phase. Before encystment, the chondriosomes divide repeatedly transversel}' and become spherical bodies which persist during encystment and in the gametes. In zygotes, these spherical bodies fuse to produce longer forms which break up into elongate filamentous structures. Richardson and Horning further succeeded in bringing about division of the chondriosomes in Opalina by changing pH of the medium. As to the function of chondriosomes, opinions vary. A number of observers hold that they are concerned with the digestive process. After studying the relationship between the chondriosomes and food vacuoles of Amoeba and Paramecium, Horning suggested that the chondriosomes are the seat of enzyme activity and it is even probable that they actually give up their own substance for this
purpose.

Mast

(1926) described "beta granules" in

Amoeba

proteus

which are more abundantly found around the contractile vacuole. Mast and Doyle (1935, 1935a) noted that these spherical to rod-like beta granules are plastic and stain like chondriosomes and that there is a direct relation between the number of beta granules in the cytoplasm and the frequency of contraction of the contractile vacuole. They maintained that these granules "probably function in transferring substances from place to place in the cytoplasm." Similar
granules are recognizable in the species of Pelomyxa (Andresen,

Kudo, 1951). The view that the chondriosomes may have something to do with the cell-respiration expressed by Kingsbury was further elaborated by Joyet-Lavergne through his studies on certain Sporozoa. That
1942; Wilber, 1942;

the chondriosomes are actively concerned with the development of the gametes of the Metazoa is well known. Zweibaum's observation,

showing an increase

in the

amount

of fatty acid in

Paramecium

just

prior to conjugation, appears to suggest this function.

On

the other

hand, Calkins found that in Uroleptus, the chondriosomes became abundant in exconjugants, due to transformation of the macronuclear material into the chondriosomes. The author agrees with McBride and Hewer who wrote: "it is a remarkable thing that so little is known positively about one of the 'best known' protoplasmic inclusions" (Piney, 1931). Condriosomes in Protozoa (MacLennan,
1941; Grasse, 1952).

MORPHOLOGY

83

Numerous minute granules, less than l^u in diameter, occur usually abundantly suspended in the cytoplasm. They can most clearly be noted under phase microscope. Mast named those found in Amoeba
"alpha granules."
Contractile

and other vacuoles

Protozoa possess one or more vacuoles known as pulsating or contractile vacuoles. They occur regularly in all freshwater-inhabiting Sarcodina, Mastigophora and Ciliophora. Marine or parasitic Sarcodina and Mastigophora do not ordinarily have a contractile vacuole. This organelle is present with a few exceptions in all marine and parasitic Ciliophora, while it is wholly absent in
of

The majority

Sporozoa. In various species of free-living amoebae, the contractile vacuole

is

formed by accumulation

of

water in one or more droplets which

continuously until
it

finally fuse into one. It enlarges itself

reaches

maximum
The

size (diastole)

and suddenly bursts through the thin

is

cytoplasmic layer above

side.

location of the vacuole

it

therefore,

discharging its content to outnot definite in such forms and, moves about with the cytoplasmic movements; and, as
it (systole),

a rule,

it is

confined to the temporary posterior region of the body.

in form,
it

Although almost spherical

in shape, as in

may

occasionally be irregular

Amoeba

striata (Fig. 184, /).

In

many

testaceans and

heliozoans, the contractile vacuoles which are variable in

are formed in the ectoplasm

number, and the body surface bulges out above

the vacuoles at diastole. In Mastigophora, the contractile vacuole

appears to be located in the anterior region. In the Ciliophora, except Protociliata, there occur one to many contractile vacuoles, which seem to be located in the deepest part of the ectoplasm and therefore constant in position. Directly above each vacuole is found a pore in the pellicle, through which the content of the vacuole
is

discharged to outside. In the species of Conslit

chophthirus, Kidder (1934) observed a narrow

just posterior to the vacuole

in the pellicle

margin
the

of the slit

is

on the dorsal surface (Fig. 27). The thickened and highly refractile. During diastole,
slit

slit is

nearly closed and, at systole, the wall of the contractile

vacuole appears to break and the content pouring out slowly.

opens suddenly, the vacuolar is only one contractile vacuole, it is usually located either near the cytopharynx or, more often, in the posterior part of the body. When several to many vacuoles are present, they may be distributed without apparent order, in linear series, or along the body outline. When the contrac-

When

there

84
tile

PROTOZOOLOGY
vacuoles are deeply seated, there
is

a delicate duct which con-

nects the vacuole with the pore on the pellicle as in

woodruffi, or in

Paramecium
etc.,

Ophryoscolecidae. In Balantidium, Nyctotherus,

is

formed very close to the permanent cytopyge located at the posterior extremity, through which it empties its
the contractile vacuole
content.

In a

besides the

number of ciliates there occur radiating or main contractile vacuole. These canals
is

collecting canals

radiate from the

etc.

central vacuole in

Paramecium, Frontonia, Disematostoma,

But

when the vacuole

radiate, in
different species:

terminal, the collecting canals of course do not

which case the number of the canals varies among one in Spirostomum, Stentor, etc., 2 in Clima-

i
a
Fig. 27.
oles

Diagrams showing the contractile vacuole, the accessory vacuand the aperture, during diastole and systole in Conchophthirus

(Kidder).

costomum, Eschaneustyla,

etc.,

and several

in Tillina. In Peritricha,

the contractile vacuole occurs near the posterior region of the cyto-

pharynx and its content is discharged through a canal into the vestibule and in Ophrydium ectatum, the contractile vacuole empties its content into the cytopharynx through a long duct (Mast). Of numerous observations concerning the operation of the contractile vacuole, that of King (1935) on Paramecium multimicronucleatum (Figs. 28, 29) may be quoted here. In this ciliate, there are 2 to 7 contractile vacuoles which are located below the ectoplasm on the aboral side. There is a permanent pore above each vacuole. Leading to the pore is a short tube-like invagination of the pellicle, with inner end of which the temporary membrane of the vacuole is in contact (Fig. 28, a). Each vacuole has 5-10 long collecting canals with strongly osmiophilic walls (Fig. 29), in which Gelei (1939) demonstrated longitudinal fibrils, and each canal is made up of terminal portion, a proximal injection canal, and an ampulla between them. Surrounding the distal portion, there is osmiophilic cytoplasm which may be granulated or finely reticulated, and

MORPHOLOGY

85

which Nassonov (1924) interpreted as homologous with the Golgi apparatus of the metazoan cell. The injection canal extends up to the pore. The ampulla becomes distended first with fluid transported discontinuously down the canal and the fluid next moves into the injection canal. The fluid now is expelled into the cytoplasm just beneath the pore as a vesicle, the membrane of which is derived from that which closed the end of the injection canal. These fluid

060 <A>
<3^=> _i^_

_5=
;

Fig. 28. Diagrams showing the successive stages in the formation of the contractile vacuole in Paramecium multimicronucleatum (King) upper figures are side views; lower figures front views; solid lines indicate permanent structures; dotted lines temporary structures, a, full diastole; b-d, stages of systole; e, content of ampulla passing into injection canal; f, formation of vesicles from injection canals; g, fusion of vesicles to form contractile vacuole; h, full diastole.

vesicles coalesce presently to

diastole

form the contractile vacuole in full and the fluid is discharged to exterior through the pore, which becomes closed by the remains of the membrane of the discharged vacuole. In Haptophrya michiganensis, MacLennan (1944) observed that accessory vacuoles appear in the wall of the contractile canal which extends along the dorsal side from the sucker to the posterior end,
as the canal contracts (Fig. 30)
.

The canal

wall expands and enlarg-

by a full expansion of the canal. Through several excretory pores with short ducts the content of the contractile canal is excreted to the exterior. The function of the contractile vacuole is considered in the following
ing accessory vacuoles fuse with one another, followed

86

PROTOZOOLOGY

Contractile vacuoles of Paramecium multimicronucleatum, c, coma, early systole, side view; b, diastole, front view; plete systole, front view; d, systole, side view.
Fig. 29.

X1200 (King),

MORPHOLOGY
chapter
(p. 118).

87

Comparative study

of contractile

vacuoles (Haye,

1930; Weatherby, 1941). Various other vacuoles or vesicles occur in different Protozoa. In

the ciliates belonging to Loxodidae, there are variable numbers of Miiller's vesicles or bodies, arranged in 1-2 rows along the aboral surface.

These

vesicles (Fig. 31, a-c)

vary

in

diameter from 5 to

8.5/*

Fig. 30. Excretory canal of Haptophrya michiganensis (MacLennan). an individual in side view, showing a contraction wave passing down the canal; b, successive views of the same region of the contractile canal during a full pulsatory cycle (a-c, systole; d-g, diastole); c, diagram showing a contractile wave passing from left to right between two adjacent
a,

excretory pores.

and contain a

clear fluid in

which one large spherule or several small

is

highly refractile spherules are suspended. In some, there

fila-

mentous connection between the spherules and the wall of the vesicle. Penard maintains that these bodies are balancing cell-organs and called the vesicle, the statocyst, and the spherules, the statoliths.

Another vacuole, known as concrement vacuole, is a characterorganella in Biitschliidae and Paraisotrichidae. As a rule, there is a single vacuole present in an individual in the anterior third of body. It is spherical to oval and its structure appears to be highly
istic

88

PROTOZOOLOGY

complex. According to Dogiel (1929), the vacuole is composed of a pellicular cap, a permanent vacuolar wall, concrement grains and

systems (Fig. 31, d). When the organism divides, the andaughter individual retains it, and the posterior individual developes a new one from the pellicle into which concrement grains

two

fibrillar

terior

Fig. 31. a-c, Miiller's vesicles in Loxodes

(a,

Penard;
cf,

b,

(Dogiel).

(a, b) and in Remanella (c) concrement vacuole of Blepharoprosthium centripetal fibril; eg, concrement grains; cp, cap; fw, fibrils
c,

Kahl);

d,

of wall; p, pellicle; vp, vacuolar pore; w, wall.

enter after

external pore. Dogiel believes that

statoliths.

appearing in the endoplasm. This vacuole shows no its function is sensory and has named the vacuole, the statocyst, and the enclosed grains, the
first

Food vacuoles are conspicuously present

which take
in

in the holozoic

Protozoa

organisms as food. The food vacuole is a space in the cytoplasm, containing the fluid medium which surrounds the protozoans and in which are suspended the food matter, such as various Protophyta, other Protozoa or small

whole or parts

of other

Metazoa. In the Sarcodina and the Mastigophora which do not

possess a cytostome, the food vacuoles assume the shape of the food

materials and,

when

these particles are large,

it is difficult

to

make

out the thin film of water which surrounds them.

When minute food

MORPHOLOGY
particles are taken

S9

through a cytostome, as is the case with the majority of euciliates, the food vacuoles are usually spherical and of approximately the same size within a single protozoan. In the saprozoic Protozoa, which absorb fluid substances through the body
surface, food vacuoles containing solid food, of course,

do not occur.

Chromatophores
d

Pvrenoids

Fig. 32. a, Trachelomonas hispida, X530 (Doflein); b, c, living and stained reproductive cells of Pleodorina illinoisensis, XlOOO (Merton); d-f, terminal cells of Hydrurus foetidus, showing division of chromatophore and pyrenoid (Geitler); g-i, Chlamydomonas sp., showing the division of pyrenoid (Geitler).

Chromatophore and associated organellae

In the Phytomastigina and certain other forms which are greenmany chromatophores (Fig. 32) containing chloro-

colored, one to

phyll occur in the cytoplasm.

The chromatophores vary

in

form

among
of the

different species; namely, discoidal, ovoid, band-form, rod-

fusiform, network or irregularly diffused. The color chromatophore depends upon the amount and kinds of pigment which envelops the underlying chlorophyll substance. Thus the chromatophores of Chrysomonadina are brown or orange, as they contain one or more accessory pigments, including phycochrysin, and those of Cryptomonadina are of various types of brown with
like, cup-like,

'

90

PROTOZOOLOGY

very diverse pigmentation. In Chloromonadina, the chromatophores are bright green, containing an excess of xanthophyll. In dinoflagellates, they are dark yellow or brown, because of the presence of
last of

pigments: carotin, phylloxanthin, and peridinin (Kylin, 1927), the which is said to give the brown coloration. A few species of
blue-green chromatophores for which phycois

Gymnodinium contain
cyanin

The chromatophores of Phytomonadina and Euglenoidina are free from any pigmentation, and therefore green. Aside from various pigments associated with the chromatophores, there are carotinoid pigments which occur often outside the chromatophores, and are collectively known as haematochrome.
held to be responsible.

The haematochrome occurs in Haematococcus pluvialis, Euglena Chlamydomonas, etc. In Haematococcus, it increases in volume and in intensity when there is a deficiency in phosphorus and especially in nitrogen; and when nitrogen and phosphorus are present sufficiently in the culture medium, the haematosanguinea, E. rubra,

chrome

loses its color completely

(Reichenow, 1909; Pringsheim,

to a development of carotin in

1914). Steinecke also noticed that the frequent yellow coloration of

phytomonads in moorland pools is due

(1939) noted that the

the chromatophores as a result of deficiency in nitrogen. Johnson

haematochrome granules

of

Euglena rubra be-

come

collected in the central portion instead of being scattered

throughout the body when sunlight becomes weaker. Thus this Euglena appears green in a weak light and red in a strong light. The chromatophores undergo division at the time when the organism which contains them, divides, and therefore the number of chromatophores appears to remain about the same through different generations (Fig. 32).

In association with the chromatophores are found the pyrenoids

(Fig. 32)

which are usually embedded

in

them. The pyrenoid

is

viscous structureless mass of protein (Czurda), and

pieces or grains

may

or

may

not

be covered by tightly fitting starch-envelope, composed of several which appear to grow by apposition of new material on the external surface. A pyrenoid divides when it reaches a certain

and also at the time of the division of the organism in which it As to its function, it is generally agreed that the pyrenoid is concerned with the formation of the starch and allied anabolic prodsize,

occurs.

ucts of photosynthesis. Pyrenoid (Geitler, 1926).

Chromatophore-bearing Protozoa usually possess also a stigma The stigma may occur in exceptional cases in colorless forms, as in Khawkinea, Polytomella, etc. It is ordinarily situated in the anterior region and appears as a reddish or
(Fig. 32) or eye-spot.

MORPHOLOGY

91

brownish red dot or short rod, embedded in the cortical layer of the cytoplasm. The color of the stigma is due to the presence of droplets of haematochrome in a cytoplasmic network. The stigma is incapable of division and a new one is formed de novo at the time of cell division. In many species, the stigma possesses no accessory parts, but, according to Mast (1928), the pigment mass in Chlamydomonas, Pandorina, Eudorina, Euglena, Trachelomonas, etc., is in cup-form, the concavity being deeper in the colonial than in solitary forms. There is a colorless mass in the concavity, which appears to function as a lens. In certain dinoflagellates, there is an ocellus (Fig. 127, c, d, q, h) which is composed of amyloid lens and a dark pigment mass (melanosome) that is sometimes capable of amoeboid change of form. The stigma is, in general, regarded as an organella for the perception of light intensity. Mast (192G) considers that the stigma in the Volvocidae is an organella which determines the direction of the movement.

References

Alexeieff, A.: (1928) Sur

question des mitochondries et de l'appareil de Golgi chez les protistes. Arch. Protist., 60:269.
la

(1929) Nouvelles observations sur les chondriosomes chez les protozoaires. Ibid., 65:45. Arcichovskij, V. (1905) Ueber das Zoopurpurin, ein neues Pigment der Protozoa (Blcpharisma lateritium). Arch. Protist., 6: 227. Beers, C. D.: (1946) Tillina magna: micronuclear number, etc.
,
:

Biol. Bull., 91:256.

Belar, K.: (1926) Der Formwechsel der Protistenkerne. Ergebn.

:

u.

Fortschr. Zool., 6:235. Bresslau, E. and Scremin, L. (1924) Die Kerne der Trypanosomen und ihre Verhalten zur Nuclealreaktion. Arch. Protist.,

48:509.

Brodsky, A.: (1924) Die Trichocysten der Infusorien. Arch.

Protist., 3:23. Brown, H. P.: (1945)

russ.

the structure and mechanics of the protoSc, 45:247. Brown1 V. E. (1930) The Golgi apparatus of Amoeba proteus. Biol. Bull., 59:240. (1930a) The Golgi apparatus of Pyrsonympha and Dinenympha. Arch. Protist., 71:453. (1930b) The neuromotor apparatus of Paramecium. Arch. zool. exper. gn., 70:469. Burt, R. L. (1940) Specific analysis of the genus Colpoda with special reference to the standardization of experimental material. Tr. Am. Micr. Soc, 59:414. Chadefaud, M.: (1938) Nouvelles recherches sur l'anatomie compare des Eugleniens: les Peranemines. Rev. Algol., 11:189.

On

zoan flagellum. Ohio

,
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PROTOZOOLOGY
cilies

Chatton, E. and Lwoff, A.: (1935) Les

zool. exp. gen., 77:1.

apostomes,

etc.

Arch.

and Lwoff, M.: (1929) Les infraciliature et la continuite genetique des systemes ciliaires recessifs. C. R. Acad.
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188:1190.
:

of the biology of Peranema triMicr. Sc, 91:279. Cleveland, L. R., Hall, S. R., Sanders, E. P. and Collier, J.: (1934) The woodfeeding roach Cryptocercus, its Protozoa, etc. Mem. Am. Acad. Arts. Sc, 17:185. Cushman, J. A.: (1933) Foraminifera their classification and economic use. 2 ed. Sharon, Mass. Dellinger, 0. P. (1909) The cilium as a key to the structure of contractile protoplasm. J. Morphol., 20:171. Dierks, K. (1926) Untersuchungen ueber die Morphologie und Physiologie des Stentor coeruleus. Arch. Protist., 54:1. Doflein, F. (1916) Studien zur Naturgeschichte der Protozoen. VII. Zool. Jahrb., Anat., 39:335. Dogiel, V.: (1923) Cellulose als Bestandteil des Skellettes bei einigen Infusorien. Biol. Zentralbl., 43:289. (1929) Die sog. "Konkrementenvakuole" der Infusorien als eine Statocyste betrachtet. Arch. Protist., 68:319. Dragesco, J.: (1951) Sur la structure des trichocystes du flagelle' cryptomonadine, Chilomonas Paramecium. Bull. Micr. appl., 2 ser., 1:172. Duboscq, O. and Grasse, P.-P. (1933) L'appareil parabasal des flagelles. Arch. zool. exp. gen., 63:381. Fischer, A.: (1894) Ueber die Geisseln einiger Flagellaten. Jahresb. wiss. Bot., 26:187. Geitler, L. (1926) Zur Morphologie und Entwicklungsgeschichte der Pyrenoide. Arch. Protist., 56:128. Gelei, J. v.: (1926) Zur Kenntnis des Wimperapparates. Zeitschr. ges. Anat., Abt. 1,81:530. (1932) Die reizleitenden Elemente der Ciliaten, etc. Arch. Protist., 77:152. Giese, A. C: (1938) Reversible bleaching of Blepharisma. Tr. Am. Micr. Soc, 57:77. Grasse, P.-P.: (1952) Traite de Zoologie. I. Fasc. 1. Paris. Haeckel, E.: (1868) Monographic der Moneren. Jen. Zeit. Natur-

Chen, Y. T. (1950) Investigations

chophorum. Quart.
J.

wiss., 4.

(1870) Studien ueber

Moneren und andere

Protisten. Leip-

zig.

Hall, R.
vital

P.: (1929) Reaction of certain cytoplasmic inclusions to dyes and their relation to mictochondria, etc. J. Morphol. Physiol., 48:105. and Nigrelli, R. F. (1937) A note on the vacuome of Paramecium bursaria and the contractile vacuole of certain ciliates. Tr. Am. Micr. Soc, 56:185. Hammond, D. M. (1937) The neuromotor system of Euplotes patella during binary fission and conjugation. Quart. J. Micr. Sc, 79:
: :

507.

MORPHOLOGY

93

and Kofoid, C. A.: (1937) The continuity of structure and function in the neuromotor system of Euplotes patella during
its life cycle.

Proc.

Am.

Phil.

Soc, 77:207.
bei

Haye, A.: (1930) Ueber den Exkretionsapparat

etc.
:

den Protisten,

Arch. Protist., 70:1. Hayes, M. L. (1938) Cytological studies on Dileptus anser. Tr. Am. Micr. Soc, 57: 11. Herfs, A. (1922) Die pulsierende Vakuole der Protozoen, etc. Arch. Protist., 44:227. Hertwig, R. (1902) Die Protozoen und die Zelltheorie. Ibid., 1:1. Hollande, A.: (1942) Etude cytologique et biologique de quelques flagelles libres. Arch. zool. exp. gen., 83:1. Horning, E. S.: (1926) Observations on mitochondria. Australian J. Exper. Biol., 3:149. (1927) On the orientation of mitochondria on the surface cytoplasm of infusorians. Ibid., 4:187. (1929) Mitochondrial behavior during the life cycle of a sporozoan (Monocystis). Quart. J. Micr. Sc, 73:135. Houwink, A. L.: (1951) An E. M. study of the flagellum of Euglena gracilis. Proc. Kon. Nederl. Ak. Weten., Ser. C, 54:132. Howland, Ruth B.: (1924) Dissection of the pellicle of Amoeba verrucosa. J. Exper. Zool., 40:263. Jacobson, Irene: (1932) Fibrillare Differenzierungen bei Ciliaten. Arch. Protist., 75:31. Jakus, Marie A.: (1945) The structure and properties of the trichocysts of Paramecium. J. Exper. Zool., 100:457. and Hall, C. E.: (1946) Electron microscope observations of the trichocysts and cilia of Paramecium. Biol. Bull., 91:141. Janicki, C: (1911) Zur Kenntnis des Parabasalapparates bei parasitischen Flagellaten. Biol. Zentralbl., 31:321. Jirovec, O. (1929) Studien ueber blepharoplastlose Trypanosomen. Arch. Protist., 68:187. Kidder, G. W. (1933) On the genus Ancistruma Strand (Ancistrum
: : :
:

Maupas).

Biol. Bull., 64:1.

(1933a) Conchophthirus caryoclada sp. nov. Ibid., 65:175. (1934) Studies on the ciliates from freshwater mussels. I, II. Ibid., 66:69, 286. King, R. L. (1935) The contractile vacuole of Paramecium multimicronucleatum. J. Morphol., 58:555. Kirby, H. Jr.: (1931) The parabasal body in trichomonad flagellates. Tr. Am. Micr. Soc, 50:189. Klein, B. M.: (1926) Ueber eine neue Eigentumlichkeit per Pellicula von Chilodon uncinatus. Zool. Anz., 67:160. (1926a) Ergebnisse mit einer Silbermethode bei Ciliaten.
:

Arch. Protist., 56:243. (1927) Die Silberliniensysteme der Ciliaten. Ibid., 58:55. (1928) Die Silberliniensysteme der Ciliaten. Ibid., 60:55 and 62:177. (1929) Weitere Beitrage zur Kenntnis des Silberliniensystems der Ciliaten. Ibid., 65: 183.

94

PROTOZOOLOGY

(1930) Das Silberliniensystem der Ciliaten. IV. Ibid., 69: 235. (1942) Differenzierungsstufen des Silberlinien- oder neuroformativen Systems. Ibid., 96:1. Kleinschmidt, A. and Kinder, E.: (1950) Elektronenoptische Befunde an Rattentrypanosomen. Zentralbl. Bakt. I Abt. Orig., 156:219. Kofoid, C. A. and Swezy, Olive: (1921) The free-swimming unarmored Dinoflagellata. Mem. Uni. Cal., 5:1. Koltzoff, N. K. (1911) Untersuchungen ueber die Kontraktilitat des Stieles von Zoothamnium alternans. Biol. Zeitschr. Moskau, 2:55. Kraneveld, F. C, Houwink, A. L. and Keidel, H. J. W. (1951) Electron microscopical investigations on trypanosomes. I. Proc.
: :

Kon. Nederl. Akad. Wetensch., C, 54:393.

Kruger,

F.:

(1934)

Bemerkungen

iiber

Flagellatentrichocysten.

Arch. Protist., 83:321. (1936) Die Trichocysten der Ciliaten im Dunkelfeld. Zoologica, 34 (H. 91) :1. Kudo, R. R.: (1924) A biologic and taxonomic study of the Microsporidia. Illinois Biol. Monogr., 9:80. (1936) Studies on Nyctotherus ovalis Leidy, etc. Arch. Protist., 87:10. (1946) Pelomyxa carolinensis Wilson. I. J. Morphol., 78:317. (1951) Observations on Pelomyxa illinoisensis. Ibid., 88: 145. Kylin, H.: (1927) Ueber die karotinoiden Farbstoffe der Algen. Zeitschr. physiol. Chem., 166:39. Lund, E. E.: (1933) A correlation of the silverline and neuromotor systems of Paramecium. Univ. Cal. Publ. Zool., 39:35. Lynch, J. E.: (1930) Studies on the ciliates from the intestine of Strongylocentrotus. II. Ibid., 33:307. MacLennan, R. F. (1941) Cytoplasmic inclusions. In: Calkins and Summers' Protozoa in biological research. (1944) The pulsatory cycle of the contractile canal in the ciliate Haptophrya. Tr. Am. Micr. Soc, 63:187. Mainx, F.: (1928) Beitrage zur Morphologie und Physiologie der Eugleninen. Arch. Protist., 60:305. Mast, S. O.: (1926) Structure, movement, locomotion and stimulation in Amoeba. J. Morphol., 41:347. (1928) Structure and function of the eye-spot in unicellular and colonial organisms. Arch. Protist., 60:197. (1944) A new peritrich belonging to the genus Ophrydium. Tr. Am. Micr. Soc, 63:181. and Doyle, W. L. (1935) Structure, origin and function of cytoplasmic constituents in Amoeba proteus. Arch. Protist., 86:
: :

155.

(1935a)

II. Ibid.,

86:278.

Moses, M. J.: (1950) Nucleic acids and proteins of the nuclei of Paramecium. J. Morphol., 87:493. Nassonov, D.: (1924) Der Exkretionsapparat (kontractile Vacuole)

MORPHOLOGY

95

der Protozoen als Homologen des Golgischen Apparatus der Metazoenzelle. Arch. mikr. Anat., 103:437. (1925) Zur Frage ueber den Bau und die Bedeutung des Lipoiden Exkretionsapparates bei Protozoen. Ztschr. Zellforsch., 2:87. Owen, H. M.: (1947) Flagellar structure. I. Tr. Am. Micr. Soc, 66:
50.

(1949)
:

II. Ibid.,

68:261.

Park, O. (1929) The osmiophilic bodies of the protozoans, Stentor and Leucophrys. Ibid., 48:20. Penard, E.: (1922) Etudes sur les infusoires d'eau douce. Geneva. Petersen, J. B. (1929) Beitrage zur Kenntnis der Flagellatengeisseln. Bot, Tidsskr., 40:373.

Pickard, Edith A.: (1927) The neuromotor apparatus

teredinidi Nelson, etc. Univ. Cal. Publ. Zool., 29:405.

of Boveria

Piekarski, G.: (1949) Blepharoplast und Trypaflavinwirkung bei

Trypanosoma

brucei. Zentralbl. Bakt., Orig., 153:109.

Piney, A.: (1931) Recent advances in microscopy. London. Pitelka, Dorothy R. (1949) Observations on flagellum structure in Flagellata. Univ. Cal. Publ. Zool., 53:377. Pollister, A. W. and Leuchtenberger, Cecilie: (1949) The nature of the specificity of methyl green for chromatin. Proc Nat. Acad. Sc, 35:111. Pringsheim, E. (1914) Die Ernahrung von Haematococcus pluvialis.
: :

Beitr. Biol. Pflanz., 12:413. Puytorac, P. de: (1951) Sur la presence d'un argyrome chez quelques cilies astomes. Arch. zool. exper. gen., 88 (N.-R.):49.

Reichenow,

E.: (1909) Untersuchungen an Haematococcus pluvialis,

Arb. kaiserl. Gesundh., 33:1. (1928) Ergebnisse mit der Nuklealfarbung bei Protozoen. Arch. Protist., 61:144. Richardson, K. C. and Horning, E. S.: (1931) Cytoplasmic structures in binucleate opalinids with special reference to the Golgi apparatus. J. Morphol. Physiol., 52:27. Roskin, G.: (1923) La structure des mvonemes des infusoires. Bull. biol. France et Belg., 57:143. (1925) Ueber die Axopodien der Heliozoa und die Greiftentakel der Ephelotidae. Arch. Protist,, 52:207. and Levinsohn, L. B.: (1929) Die Kontractilen und die Skelettelemente der Protozoen. I. Ibid., 66:355. Rumjantzew, A. and Wermel, E. (1925) Untersuchungen ueber den Protoplasmabau von Actinosphaerium eichhorni. Ibid., 52:
etc.
:

217.

Saunders, J. T.: (1925) The trichocysts of Paramecium. Proc. Cambridge Philos. Soc, Biol. Sc, 1:249. Schroder, O.: (1906) Beitrage zur Kenntnis von Stentor coeruleus

und St. roeselii. Arch. Protist,, 8:1. Schuberg, A.: (1888) Die Protozoen des Wiederkauermagens.
Zool. Jahrb., Abt. Syst,, 3:365.
:

I.

Sharp, R. (1914) Diplodinium ecaudatum with an account of its neuromotor apparatus. Univ. California Publ. Zool., 13:43.

96

PROTOZOOLOGY

oligotriche Infusorien aus dem Darme des Pferdes. I. Arch. Protist., 68:503. Taylor, C. V.: (1920) Demonstration of the function of the neuromotor apparatus in Euplotes by the method of micro-dissection. Univ. California Publ. Zool., 19:403. (1941) Ciliate fibrillar systems. In: Calkins and Summers' Protozoa in biological research. ten Kate, C. G. B.: (1927) Ueber das Fibrillensvstem der Ciliaten. Arch. Protist., 57:362. (1928) II. Ibid., 62:328. Thon, K. (1905) Ueber den feineren Ban von Didinium nasutum. Ibid., 5:282. Tobie, Eleanor J.: (1951) Loss of the kinetoplast in a strain of Trypanosoma equiperdum. Tr. Am. Micr. Soc, 70:251. Tonniges, C: (1914) Die Trichocysten von Frontonia leucas und ihr chromidialer Ursprung. Arch. Protist., 32:298. Turner, J. P.: (1933) The external fibrillar system of Euplotes with notes on the neuromotor apparatus. Biol. Bull., 64:53. (1937) Studies on the ciliate Tillina canalifera n. sp. Tr.
:

Strelkow, A.: (1929) Morphologische Studien ueber

Am.

Micr. Soc, 56:447.

(1940) Cytoplasmic inclusions in the ciliate, Tillina canalifera. Arch. Protist., 93:255.

(1903) Allgemeine Physiologic 4th ed. Jena. P.: (1926) Feeding reactions in the ciliate Dileptus gigas, etc Biol. Bull., 45: 113. Vlk, W.: (1938) Ueber den Bau der Geissel. Arch. Protist., 90:-148. Weatherby, J. H.: (1941) The contractile vacuole. In: Calkins and

Verworn, M.:
Visscher,
J.

Summers' Protozoa in biological research. Weisz, P. B.: (1948) The role of carbohydrate reserves in the regeneration of Stentor fragments. J. Exper. Zool., 108:263. (1949) A cytochemical and cytological study of differentiation in normal and reorganizational stages of Stenlor coeruleus. J. Morphol., 84:335. (1950) On the mitochondrial nature of the pigmented granules in Stentor and Blepharisma. Ibid., 86:177. Wetzel, A.: (1925) Vergleichend cytologische Untersuchungen an Ciliaten. Arch. Protist., 51:209. Wilber, C. G. (1942) The cytology of Pelomyxa carolinensis. Trans. Am. Micr. Soc, 61:227. (1945) Origin and function of the protoplasmic constituents in Pelomyxa carolinensis. Biol. Bull., 88:207. Wohlfarth-Bottermann, K-E. (1950) Funktion und Struktur der Parameciumtrichocysten. Wissenschaften, 37:562. Woodcock, H. M.: (1906) The haemoflagellates a review of present knowledge relating to the trypanosomes and allied forms. Quart. J. Micr. Sc, 50:151. Woodruff, L. L. and Spencer, H.: (1922) Studies on Spathidium spatula. I. Jour. Exp. Zool., 35:189. Yocom, H. B. (1918) The neuromotor apparatus of Euplotes patella. Univ. California Publ. Zool., 18:337.
:

Chapter

Physiology
morphological consideration which has THE chapter, though
last
is,

been given in the

necessarily brief, indicative of the occur-

rence of various and often complex organellae in Protozoa.

physiological activity of the whole protozoan
all
is

The

the sum-total of

the functions which are carried on by numerous minute parts or

cell

organellae of the

body, unlike the condition found in a metazoan. (1933) stated, "physiological problems (of Protozoa) for the most part begin where similar problems of the Metazoa leave off, namely the ultimate processes of the single cell. Here the functional activities have to do with the action and interIndeed,
as

Calkins

action of different substances which enter into the

make-up

of

protoplasm and, for the most part, these are beyond our powers of analysis." A full discussion of various physiological problems pertaining to Protozoa
fore,
is out of question in the present work and, therea general consideration on protozoan physiology will suffice

for our purpose.

Nutrition

Protozoa obtain nourishment in manifold ways. Information on the nutrition of the Protozoa is undergoing an accelerated progress through improvements in technique in experimental cultivation. In

many Phytomastigina

(Pringsheim, 1937a; Hall, 1939), afewciliates

(Kidder and Dewey, 1951) and many blood-inhabiting flagellates (Lwoff, 1951) which have been cultivated in vitro free from other organisms, a much clearer information is becoming available. But for the majority of Protozoa a thorough comprehension of the nutrition is to be sought in future (Doyle, 1943; Lwoff, 1951; Most, 1951;
Kidder, 1951). Holozoic (zootrophic, heterotrophic) nutrition. This
is

the

method

higher animals obtain their nourishment; namely, the protozoan uses other animals or plants as sources of food. It involves

by which

all

the food-capture and ingestion, digestion and assimilation, and rejection of indigestible portions.

The methods of food-capture vary among different forms. In the Sarcodina, the food organisms are captured and taken into the body at any point. The methods however vary. According to Rhumbler's
(1910) oft-quoted observations, four
;

methods

of food-ingestion oc-

cur in amoebae (Fig. 33) namely, (1) by "import," in which the food is taken into the body upon contact, with very little movement on
97

. ;

98

PROTOZOOLOGY

amoeba (a); (2) by "circumfluence,'' in which the cytoplasm flows around the food organism as soon as it comes in contact with it on all sides and engulfs it (6) (3) by "circumvallation," in which the amoeba without contact with the food, forms pseudopodia which surround the food on all sides and ingest it (c)
the part of the
;

a,

Fig. 33. Various ways by which amoebae capture food organisms, A moeba verrucosa feeding on Oscillatoria by 'import' (Rhumbler) b, A proteus feeding on bacterial glea by 'circumfluence'; c, on Paramecium by 'circumvallation' (Kepner and Whitlock) d-h, A. verrucosa ingesting a food particle by 'invagination' (Gross-Allermann).
;
;

(4)

by "invagination,"

in

which the amoeba touches and adheres to

it is

the food, and the ectoplasm in contact with

(d-h). In a species of Hartmannella,

invaginated into the

later disappears

endoplasm as a tube, the cytoplasmic membrane

Ray

(1951) reports an aggluti-

nation of large numbers of motile bacteria over the body surface,

which

later form a large mass and are taken into a food cup. In certain testaceans, such as Gromia, several rhizopodia cooper-

ate in engulfing the prey and, in Lieberkuhnia (Fig. 34),

Verworn

noted

ciliates are

captured by and digested in rhizopodia. Similar

SIOLOGY

00

observation was made by Schaudinn in the heliozoan Camptonema in which several axopodia anastomose to capture a prey (Fig. 214, d). In the holozoic Mastigophora, such as Hypermastigina, which do not possess cytostome, the food-ingestion is by import or invagination as noted in Trichonympha campanula (Cleveland, 1925a; Emik, 1941) (Fig. 35, a) and Lophomonas blattarum (Kudo, 1926). The food particles become attached to the pseudopodium and are held there on account of the viscid nature of the pseudopodium. The sudden immobility of active organisms upon coming in contact with pseudopodia of certain forms, such as Actinophrys, Actinosphaerium, Gromia, Elphidium, etc., suggests, however, probable discharge of poisonous substances. In the Suctoria which lack a cytostome, the
tentacles serve as food-capturing organellae.

The

suctorial tentacle

Fig. 34.

Rhizopodium

of Lieberkiihnia, capturing

and digesting

Colpidium colpoda (Vervvorn).

bears on
its distal

end a rounded knob which, when

it

comes

in con-

tact with an actively

swimming

ciliate,

stops the latter immediately

(Parapodophrya typha, Fig. 369, a). The prehensile tentacles of Ephelotidae are said to be similar in structure to the axopodia, in that each possesses a bundle of axial filaments around a cytoplasmic core (Roskin, 1925). These tentacles are capable of piercing through the body of a prey. In some suctorians, such as Choanophrya (Fig. 374, a), the tubular tentacles are clearly observable, and both solid and liquid food materials are sucked in through the cavity. The rapidity with which tentacles of a suctorian stop a very actively swimming ciliate is attributed to a certain substance secreted by the tentacles, which paralyses the prey. In the cytostome-bearing Mastigophora, the lashing of flagella will aid in bringing about the food particles to the cytostome, where

100
it is

PROTOZOOLOGY
taken into the endoplasm. Chen (1950) observed Peranema feed-

ing on immobile organisms.

When

the tip of the anterior flagellum

comes

in contact

with an immobile Euglena, the whole flagellum

Fig. 35. a, eight outline sketches of a Trichonympha campanula, ingesting a large particle of food, XI 50 (Emik); b, four outline sketches of a Peranema trichophorum feeding on an immobile Euglena (Chen).

beats actively and the body contracts, followed by elongation.

process
is

The

repeated several times until the body touches Euglena.

Then the cytostome stretches open, the oral rods move up, protrude from the body and become attached to Euglena. Peranema advances

PHYSIOLOGY
toward the prey and the whole Euglena
utes (Fig. 35,
b).
is

101

engulfed in 2 to 15 min-

In the
kinds.

ciliates,

there are

many
is

types of cytostome and associated

seems to be in general of two permanently open, the organism ingests continuously food particles that are small enough to pass the cytostome and cytopharynx, as in the case of Paramecium. The other type is carried on by organisms bearing cytostome which is ordinarily closed such as seen in Coleps, Didinium, Perispira (Dewey and Kidder, 1940), but which expands to often an extraordinary size when the ingestion of prey takes place. Cannibalism in Protozoa (Dawson, 1919; Lapage, 1922; Gelei, 1925a; Tanabe and Komada, 1932; Giese and Alden, 1938; Chen, 1950). The ingested food particles are usually surrounded by a film of fluid which envelops the organism and the whole is known as the food vacuole (p. 88). The quantity of fluid taken in with the food varies greatly and, generally speaking, it seems to be inversely proportional to the size, but proportional to the activity, of the food organisms. Food vacuoles composed entirely of surrounding liquid medium have occasionally been observed. Edwards (1925) noticed ingestion of fluid medium by an amoeba by forming food-cups under changed chemical composition. Brug (1928) reports seeing Entamoeba histolytica engulf liquid culture medium by formation of liplike elevation of the ectoplasm and Kirby (1932) figures ingestion of the brine containing no visible organisms by the cytostome of Rhopalophrya salina (Fig. 36). Mast and Doyle (1934) state that if Amoeba proteus, A. dubia, A. dofleini, or A. radiosa is placed in an albumin solution, a hypertonic balanced salt solution, or a hypertonic solution of calcium gluconate it rapidly decreases in volume, and forms numerous tubes filled with fluid, which disintegrate sooner or later and release their fluid content in the cytoplasm. At times 50 or more such tubes may be present, which indicates that the organism ingests considerable quantities of fluid in this way. The two authors consider that it is "a biological adaptation which serves to compen-

organelles, but the food-capturing

When

the cytostome

sate for the rapid loss of water."

as

The food vacuoles finally reach the endoplasm and in forms such Amoebina the vacuoles are carried about by the moving endo-

ciliates, the fluid endoplasm shows often a definite movement. In Paramecium, the general direction is along the aboral side to the anterior region and down the other side, with

plasm. In the
rotation

a short cyclosis in the posterior half of the body.

Some

observers maintain that in ciliates there

is

a definite "diges-

102

PROTOZOOLOGY

cytostome and ending in the cytoit. Cosmovici (1931, 1932) saw such a canal in soluble starch-fed Colpidium colpoda upon staining with iodine, but Hall and Alvey (1933) could not detect such a structure in the same organism. Kitching (1938b) observed no such tubule in the peritrichous ciliates he studied, and concluded that the food vacuoles are propelled over the determined part of the course by the contraction of surrounding cytoplasm. In Vorticella sp., food vacuoles are formed one by one at the end of cytopharynx, migrate through different parts of the cytoplasm without order and food material is digested (Fig. 37, a). Old food vacuoles are defecated through a small papilla on the lower wall of the cytopharynx and thence to the outside (Hall and Dunihue, 1931) (Fig. 37, b-d).
tive tubule" beginning with the

pyge, and the food vacuoles travel through

^r\

n
is

tr\

n n
(Kirbj').

Fig. 36. Ingestion of brine

by Rhopalophrya salina

As stated above, in a number of species the food organisms are paralyzed or killed upon contact with pseudopodia, tentacles or exploded trichocysts. In numerous other cases, the captured organism
be noted by obAmoeba proteus or actively moving bacteria ingested by Paramecium. But the prey ceases to move in a very short time. It is generally believed that some substances are secreted into the food vacuole by the protoplasm of the organisms to stop the activity of the prey within the food vacuole. Engelmann (1878) demonstrated that the granules of blue litmus, when ingested by Paramecium or Amoeba, became red in a few minutes. Brandt (1881) examined the staining reactions of amoebae by means of

taken into the food vacuole

alive, as will easily

serving Chilomonas taken in by

haematoxylin, and found that the watery vacuoles contained an Metschnikoff (1889) also showed that there appears an acid secretion around the ingested litmus grains in Mycetozoa. Greenacid.

wood and Saunders

(1894) found in Carchesium that ingestion of

PHYSIOLOGY

103

food particles stimulated the cytoplasm to secrete a mineral acid. According to Nirenstein (1925), the food vacuole in Paramecium undergoes change in reaction which can be grouped in two periods.

The first is acid reaction and the second alkaline reaction, in which albumin digestion takes place. On the other hand, Khainsky (1910) observed that the food vacuole of ciliates, such as Paramecium, is

sp. (Hall

Diagrams showing movements of food vacuoles in Vorticella and Dunihue). a, diagram of the migration paths of six food vacuoles (vacuoles 1, 2, most recently formed; 3, 4, recently formed; 5, 6, formed some time before) b-d, stages in extrusion of a food vacuole (b,
Fig. 37.
;

food vacuole entering gullet; c, a later stage; d, the food vacuole leaving cytostome, while another one is moving up toward the cytopyge).

acid during the entire period of protein digestion,

tral to finally alkaline

and becomes neuis

when the

solution of the food substance

ended. Metalnikoff (1912) found that in the food vacuoles of Paramecium, besides acid-alkaline reaction change, some vacuoles never

show acid reaction and others occasionally show sustained acid

tion. Shapiro (1927) studied the reaction

reac-

change of the food vacuoles in Paramecium caudatum by using phenol red, neutral red, Congo red, and litmus, and found that when the organism is kept in a medium with pH 7, its food vacuoles are first alkaline (pH 7.6), soon reach a maximum acidity (pH 4.0), while still in the posterior

104

PROTOZOOLOGY

show a decreased acidity, finally In Vorticella sp. and Stylonychia pustulata, the range of observed in the food vacuoles was said to be 4.57.0 and 4.8-7.0 respectively. The food vacuoles of Actinosphaerium, according to Howland (1928), possess at the beginning pH
half of the body. Later, the vacuoles

reaching

pH pH

7.0.

6.0-7.0 for 5 to 10 minutes, but this soon changes to acid

in

(pH

4.3)

which digestion appears to be carried on. In older food vacuoles which are of less acid (pH 5.4-5.6), the digestion appears to be at an end. In the species of Bresslaua, Claff, Dewey and Kidder (1941) noted that a Colpoda taken into the food vacuole is instantly killed with a sudden release of an acid which shows pH 3.0-4.2. During digestion the protoplasm of the prey becomes alkaline and the undigested residue becomes acid before extrusion. Mast's observations (1942) on the food vacuoles in Amoeba proteus and A. dubia containing Chilomonas or Colpidium, indicate: (1) the fluid in the vacuoles becomes first acid and then alkaline; (2) the increase in the acidity of the fluid in the vacuole is not due to cytoplasmic secretion, but is probably due to respiration in the ingested organisms, chemical changes associated with their death, etc.; and (3) the death of the organisms taken in the food vacuoles is probably caused by the decrease in oxygen in the vacuoles, owing to the respiration of the organisms in them. De La Arena (1941, 1942) found the maximum acidity of the fluid of food vacuoles in Pelomyxa carolinensis containing Colpidium striatum was pH 5.8 and was not fatal for the ciliate, but considered the possibility of the existence in the food vacuole of "some lethal agent" which kills the prey. Just exactly what processes take place in the food vacuole have been observed only in a few cases. Nirenstein (1925) noticed the appearance of numerous neutral red-stainable granules around the food vacuole which pass into the interior of the vacuole, and regarded them as carriers of a tryptic ferment, while Roskin and Levinsohn (1926) demonstrated the oxidase reaction in these granules. Hopkins and Warner (1946) believe that the digestion of food in Entamoeba histolytica is brought about by enzymes carried to the food vacuoles by "digestive spherules" which arise at the periphery of the nucleus, apparently due to the action of the substances diffusing from the nucleus into the cytoplasm.

As to the

localization or distribution of
is

enzymes within protozoan

body, definite information

not yet available. In centrifuged

proteus, Holter and Kopac (1937) found the peptidase acindependent of all cytoplasmic inclusions that were stratified by centrifugal forces. Holter and L0vtrup (1949) found peptidase in
tivity

Amoeba

PHYSIOLOGY
after centrifugation, possibly with a

105

centrifuged Pelomyxa carolinensis comparatively evenly distributed

tendency to be concentrated in
largely localized in the heavier

the lighter half, while proteinase

half in

was

which cytoplasmic granules were accumulated, and concluded that these two enzymes are bound, at least in part, to different cytoplasmic components. A number of enzymes have been reported to occur in Protozoa, some of which are listed in Table 3. These findings suffice to indicate that the digestion in Protozoa is carried on also by enzymes and its course appears to vary among different Protozoa. The albuminous substances are digested and decomposed into simpler compounds by enzymes and absorbed by the surrounding cytoplasm. The power to digest starch into soluble sugars is widely found among various Protozoa. It has been reported in Mycetozoa, Foraminifera, Pelomyxa, Amoeba, Entamoeba, Ophryoscolecidae and other ciliates by several investigators. The members of Vampyrella (p. 420) are known to dissolve the cellulose wall of algae, especially Spirogyra in order to feed on their

Pelomyxa (Stole), Foraminifera (Schaudinn), Amoeba (Rhumbler), Hypermastigina, Polymastigina (Cleveland), etc., have also been known for possessing the power of cellulose digestion. Many of the Hypermastigina and Polymastigina which lead symbicontents.
otic life in the intestine of the termite

onstrated by Cleveland and his co-workers, digest

cellulose

and of the wood roach, as demby enzymes the

which the host insect ingests. The assimilation products produced by an enormous number of these flagellates are seemingly sufficient to support the protozoans as well as the host. The ciliate commensals inhabiting the stomach of ruminants also apparently digest the cellulose, since the faecal matter as a rule does not contain this substance (Becker et al., 1930; Weineck, 1934).

Dawson and Belkin

found

(1928) injected oils into

Amoeba dubia and

by Amoeba
proteus

1.4 to 8.3 per cent digested.

Mast

(1938) reported that the

neutral fat globules of Colpidium are digested

and transformed into fatty acid and glycerine which unite and form neutral fat. Chen (1950) found that when Peranema trichophorum was fed on almond oil (stained dark blue with Sudan black), Sudan
III-stainable droplets gradually increased in

number

in five to 10

and considered that the droplets were "fat-substances" resynthesized from products of digestion of almond oil by this flagellate. The digestion of
hours, while ingested oil-droplets decreased in size,
rice starch is

followed

by the appearance

of increasing

number

of

ovoid paramylon granules, and the digestion of casein results in the

formation of

oil

droplets and paramylon bodies.

106

PHYSIOLOGY
carbohydrate metabolism
proportionate to the
of the

107

organism, since their number was

amount of food obtained by the organism. Veley (1905) on the other hand found them albuminoid in nature. Studies of the refringent bodies in Amoeba proteus led Mast and Doyle (1935, 1935a) to conclude that the outer layer is composed of a protein stroma impregnated with lipid containing fatty acid, which
gives positive reaction for Golgi substance; the envelope
of a
is

made up

carbohydrate which

is

neither starch nor glycogen; and the re-

fringent bodies function as reserve food, since they disintegrate dur-

The same function was assigned to those occurring in Pelomyxa carolinensis by Wilber (1945, 1945a), but Andresen and Holter (1945) do not agree with this view, as they observed the number of the refringent bodies ("heavy spherical bodies") remains the same in starvation. Thus a full comprehension of the nature and function of the refringent body must depend on future observations. The indigestible residue of the food is extruded from the body. The extrusion may take place at an}' point on the surface in many
ing starvation.

Sarcodina by a reverse process of the ingestion of food. But in

pelli-

cle-bearing forms, the defecation takes place either through the

cytopyge located

in the posterior region of the

body

or through an

aperture to the vestibule (Fig. 37, b-d). Permanent cytopyge is lacking in some forms. In Fabrea salina, Kirby (1934) noticed that a large

formed at the posterior end, the contents of food vacuoles and the opening closes over. At first the margin of the body is left uneven, but soon the evenly rounded outline is restored. The same seems to be the case with Spirostomum (Fig. 38), Blepharisma, etc. Cytopyge (Klein, 1939).
opening
is

are discharged,

of nutrition in

Holophytic (autotrophic, prototrophic) nutrition. This is the type which the Protozoa are able to decompose carbon

dioxide
in the

by means of chlorophyll contained in chromatophores (p. 89) presence of the sunlight, liberating the oxygen and combining
Aside from the Phytomastigina, chromato-

the carbon with other elements derived from water and inorganic
salts (photosynthesis).

phores were definitely observed in a ciliate Cyclotrichium meunieri (Figs. 300, o; 301) (Powers, 1932; Bary and Stuckey, 1950). In a

number
but
is

of other cases, the organism itself is without chromatophores, apparently not holozoic, because of the presence of chlorophyll-bearing organisms within it. For example, in the testacean

Paulinella (Fig. 206, c) in which occur no food vacuoles, chromatophores of peculiar shape are always present. The latter appear to be

a species of alga which holds a symbiotic relationship with the

testacean, and perhaps acts for the sarcodinan as the chromatophores

108
of the

PROTOZOOLOGY
Phytomastigina.

A similar relationship seems to exist between

and zoochlorellae;
(p.

Paramecium

bursaria, Stentor pohjmorphus, etc.

Paraeuplotes tortugensis and a zooxanthella and others

29).

Pringsheim (1928) showed that organic matters from zoochlorellae are passed on to their host, Paramecium bursaria, to be used as food.

Through studies of relationships between zooxanthellae and inYonge observed that the zooxanthellae utilize carbon dioxide, nitrogen and phosphorus which are the catabolic products of the host and supply in return oxygen, fats and carbohydrates to the host. Photosynthesis in Phytomastigina (Hutner and Provasoli,
vertebrates,
1951).

Saprozoic (saprophytic) nutrition. In this nutrition, the Protozoa

obtain nourishment by diffusion through the body surface. This
is

accomplished without any special organellae. Perhaps the only

in-

Fig. 38. Outline sketches showing the defecation process in Spirostomum ambiguum (Blattner).

stance in which the saprozoic nutrition

special organella
is

is

accomplished through a

the pusules (Figs. 127, 129) in marine dinoflagel-

lates which, according to

tain

Kofoid and Swezy (1921), appear to condecomposed organic matter and aid the organisms in carrying
originate

on this process.

The dissolved food matters are simpler compounds which

in

animal or vegetable matter due to the decomposing activities of bacterial organisms. Numerous free-living flagellates nourish themselves with this method. Recently a number of investigators found that saprozoic Protozoa could be cultivated in bacteria-free media of known compositions. For example, Pringsheim (1937) observed in Polytoma uvella (Fig. 113, h) that sodium acetate is needed from which the starch among others is produced and carbohydrates have no direct bearing upon the nutrition, but fatty acids derived from them participate in the metabolism. The Protozoa which live within the body of another organism are

PHYSIOLOGY
able to nourish themselves

109
or

by absorbing the digested

decomposed

substances of the host and could be considered assaprozoic, though the term parasitic has sometimes been used. Coelozoic Protozoa belong to this group, as for example, Protociliata, astomatous
ciliates,

In the case of cytozoic or certain histozoic forms, such as Cnidosporidia, the host cytoplasm is apparently
etc.

Trypan osomatidae,
liquefied or

hydrolyzed by enzymes before being absorbed by them. which actually feed on host tissue cells, such as Entamoeba histolytica, Balantidium coli, etc., or endo commensals, {Endamoeba blattae, Entamoeba coli, etc.) employ, of course, the holo-

The

parasitic Protozoa,

zoic nutrition.

Protozoa nourish themselves by more than one method at or different times, subject to a change in external conditions. This is sometimes referred to as mixotrophic nutrition (Pfeiffer). For example, Euglena gracilis, according to Zumstein (1900), Lwoff (1932) and Pringsheim and Hovasse (1948), loses its green coloration in the darkness or even in the light when the culture medium is very abundant in decomposed organic substances, which may indicate that this organism is capable of carrying on both holothe

Many

same

phytic and saprozoic nutrition.

With the introduction of bacteria-free culture technique in recent it has now become well established that a protozoan species exhibits conspicuous differences in form, size and structure, which are exclusively due to differences in the kind and amount of food material. For example, Kidder, Lilly and Claff (1940) noted in
years,

Tetrahymena vorax

(Fig.

39), bacteria-feeders are tailed (50-75^

long), saprozoic forms are fusiform to ovoid (30-70/x long),

forms

feeding on sterile dead ciliates are fusiform (60-80^ long), and carni-

vores and cannibals are irregularly ovoid (100-250^ long), in the latter

form of which a large "preparatory vacuole" becomes developed. In Chilomonas Paramecium, Mast (1939) observed the individuals grown in sterile glucose-peptone solution were much smaller than those cultured in acetate-ammonium solution and moreover the former contained many small starch grains, but no fat, while the latter showed many larger starch grains and a little fat. Amoeba proteus when fed exclusively on Colpidium, became very large and extremely "fat" and sluggish, growing and multiplying slowly, but indefinitely; when fed on Chilomonas only, they grew and multiplied for several days, then decreased in number and soon died, but lived longer on Chilomonas cultured in the glucose-peptone. It is well known that Protozoa as any other organism, show atypical or abnormal morphological and physiological peculiarities. In the

110

PROTOZOOLOGY
may
pro-

case of carnivorous forms, the condition of food organisms

duce abnormalities in them, as was shown by Beers (1933) in Didinium fed on starved paramecia (Fig. 40). Some thirty years ago, Robertson (1921-1927) reported that when two ciliates, Enchelys and Colpoda, are placed in a small amount of
fresh culture

medium, the

rate of reproduction following a "lag pe-

Fig. 39. Form and size variation in Tetrahymena vorax, due to differences in kind and amount of food material, as seen in life, X400 (Kidder, Lilly and Claff). a, bacteria-feeder; b, c, saprozoic forms; d, individual which has fed on killed Colpidium campylum; e, starved individual from a killed-Colpidium culture; f-i, progressive form and size changes of saprozoic form in the presence of living Colpidium; j, a young carnivore which has been removed to a culture with living yeast.

PHYSIOLOGY
riod"

111

is more than twice (up to ten times) that of a single animal in same amount of the medium. He assumed that this acceleration was due to a certain agent or substance produced within the animal,

the

Fig. 40. Didinium nasutum, X265 (Beers), a, normal fully grown animal; b-e, abnormal organisms which were fed on starved Paramecium.

which diffused into the culture medium.

is

When more

than one animal

substance
is

confined in a limited

amount

of culture fluid, this

present in a higher concentration than with one animal, and an increased rate of division
catalytic result,"
is the result. Robertson called this and the phenomenon, "allelocatalysis."

"allelo-

112

PROTOZOOLOGY

Soon a large number of observers came forward with varying resome confirmatory, others contradictory. The vast majority of these observations including Robertson's own, were carried on ciliates which were grown in association with various bacteria, and naturally, the results lacked agreement. For a review of these observations too numerous to mention here, the reader is referred to Allee (1931, 1934), Mast and Pace (1938) and Richards (1941). When bacteria-free cultivation became possible for some Protozoa, it was hoped that this problem might be solved under controlled conditions. How ever, the results still lack agreement. For example, Phelps (1935) reported that in Tetrahymena (Glaucoma), the growth rate and the maximum yield were the same between tw o cultures: one started with 0.014 organism and the other, with 1600 organisms per ml. Thus there was no allelocatalysis. On the other hand, Mast and Pace (1938) noted a significant acceleration of the growth rate in Chilomonas when up to 50 organisms were inoculated into 0.4 cc. of culture fluid as compared to the growth rate in cultures with one or more Chilomonas inocula, and furthermore, a single Chilomonas showed an increased rate of reproduction as the volume of the culture fluid was reduced.
sults

Various aspects of metabolic processes

tors,

in

Protozoa such as inor-

ganic requirements, carbon and nitrogen metabolism, growth fac-

vitamins,

vestigators.

etc., have recently been studied by a number of inFor information, the reader is referred to Hall (1941)

and Lwoff (1951).

Reserve food matter

The anabolic activities of Protozoa result in the growth and increase in the volume of the organism, and also in the formation and
storage of reserve food-substances which are deposited in the cy-

toplasm to be utilized later for growth or reproduction. The reserve food stuff is ordinarily glycogen or glycogenous substances, which seem to be present widely. Thus, in saprozoic Gregarinida, there occur in the cytoplasm numerous refractile bodies which stain

brown to brownish-violet in Lugol's solution; are insoluble in cold water, alcohol, and ether; become swollen and later dissolved in boiling water; and are reduced to a sugar by boiling in dilute sulphuric acid. This substance which composes the refractile bodies is called paraglycogen (Biitschli) or zooamylon. Gohre (1943) considers it a
stabilized polymerization product of glycogen.

Rumjantzew and Wermel

(1925) demonstrated glycogen in Acis

tinosphaerium. In the cysts of Iodamoeba, glycogen body

con-

PHYSIOLOGY
spicuously present and
is

113

looked upon as a characteristic feature of

The iodinophile vacuole of the spores of Myxobolidae a well-defined vacuole containing glycogenous substance and is also considered as possessing a taxonomic value. In many ciliates, both free-living (Paramecium, Glaucoma, Vorticella, Stentor, etc.) and parasitic (Ophryoscolecidae, Nyctotherus, Balantidium (FaureFremiet and Thaureaux, 1944)), glycogenous bodies are always present. According to MacLennan (1936), the development of the paraglycogen in Ichthyophthirius is associated with the chondriosomes. In Eimeria tenella, glycogenous substance does apparently not occur in the schizonts, merozoites, or microgametocytes but
the organism.
is
;

becomes apparent

first in

the macrogametocyte, and increases in

1944).

amount with
in

its

development, a small amount being demonstrable

al.,

the sporozoites (Edgar et

Fig. 41. a-d, (Btitschli); e-h,

two types paramylon

of
of

paramylon present

in

Euglena
(e,

gracilis

appearance;

f,

g,

sanguinea, X1100 (Heidt). dried forms; h, strongly pressed body.)

'.

natural

The anabolic products of the holophytic nutrition are starch, oil and fats. The paramylon bodies are of various forms among different species, but appear to maintain a certain characterparamylon,
istic

form within a species and can be used to a certain extent in taxonomic consideration. According to Heidt (1937), the paramylon of Euglena sanguinea (Fig. 41) is spirally coiled which confirms Butschli's observation. The paramylon appears to be a polysaccharide which is insoluble in boiling water, but dissolves in concentrated sulphuric acid, potassium hydroxide, and slowly in formaldehyde. It does not stain with either iodine or chlor-zinc-iodide and when treated with a dilute potassium hydroxide, the paramylon bodies become enlarged and frequently exhibit a concentric stratification.
is in the form which are known as leucosin, probably a carbohydrate which when boiled in water stains with iodine. Oil

In the Chrysomonadina, the reserve food material

of refractile spheroid bodies


114

PROTOZOOLOGY
when
there
is

droplets occur in various Protozoa and

of oil-producing

a large

number
develop

forms

in a

body

of water, the
4.

water

may

various odors as indicated in Table

Table
Protozoa

4.

Protozoa and odors of water

PHYSIOLOGY
coined the

115

name and held it to be made up of a nucleic acid. It stains deeply with nuclear dyes. Reichenow (1909) demonstrated that if Haematococcus pluvialis (Fig. 42) is cultivated in a phosphorus-free medium, the volutin is quickly used up and does not reappear. If however, the organisms are cultivated in a medium rich in phosphorus, the volutin increases greatly in volume and, as the culture
becomes
114,
c,

old, it

gradually breaks down. In Polytomella agilis (Fig.

d),

Doflein (1918) showed that an addition of sodium phos-

phate resulted in an increase of volutin. Reichenow, Schumacher^

Fig. 42. Haematococcus pluvialis, showing the development of volutin medium rich in phosphorus and its disintegration in an exhausted medium, X570 (Reichenow). a, second day; b, third day; c, fourth day;
in the
d, e, sixth

day;

f,

eighth day.

a special reserve food material for the nuclear substance. Sassuchin (1935) studied the volutin in Spirillum volutans and Sarcina flava and found that the volutin appears during the period of strong growth, nourishment and multiplication, disappears in unfavorable
is

and and

others, hold that the volutin appears to be a free nucleic acid,

condition of nourishment and gives a series of characteristic carbohydrate reactions. Sassuchin considers that the volutin is not related
to the nucleus, but
is

a reserve food material of the

living things,

cell,

and

is

composed

of glycoprotein. Volutin (Jirovec, 1926).

Starvation.

As in

all

perish sooner or later.

are: gradual loss of vacuoles and their coalescence, and finally the disintegration of the body. In starved Pelomyxa carolinensis, Andresen and Holter (1945) noticed the following changes: the animals disintegrate in 10-25

when deprived of food, Protozoa The changes noticeable under the microscope cytoplasmic movement, increasing number of

days at 22C. body volume decreases particularly during the early days of starvation and is about 20-30 per cent of the initial volume at the time of death; food vacuoles are extruded from the body in 24 to 48 hours; the cytoplasm becomes less viscous and many fluid vacuoles make their appearance; crystals and refringent bodies enclosed within vacuoles, form large groups as the vacuoles coalesce, some of which are extruded from the body; crystals and refringent bodies remain approximately constant during starvation and there
;

116
is

PROTOZOOLOGY

no indication that they are utilized as food reserves. The ratio of reduced weight and volume and the specific gravity remain reasonably constant during starvation (Zeuthen, 1948). Andresen (1945) found starved Amoeba proteus to show a similar change on the whole, except that the number of chondriosomes decreased and in some
cases dissolution of crystals occurred just before disintegration.

Respiration

In order to carry on various vital activities, the Protozoa, like

all

other organisms, must transform the potential energy stored in

highly complex chemical

in this process

various forms of active energy

stances in two

compounds present in the cytoplasm, into by oxidation. The oxygen involved

appears to be brought into contact with the subin Protozoa. The great majority of free-living, and certain parasitic forms absorb free molecular oxygen from the surrounding media. The absorption of oxygen appears to be carried on by the permeable body surface, since there is no special organella for this purpose. The polysaprobic Protozoa are known to live in water containing no free oxygen. For example, Noland (1927) observed Metopus es in a pool, 6 feet in diameter and 18 inches deep, filled with dead leaves which gave a strong odor of hydrogen

ways

14C, and contained no carbon dioxide, and 78.7 c.c. per liter of fixed carbon dioxide. The parasitic Protozoa of metazoan digestive systems live also in a medium containing no molecular oxygen. All these forms appear to possess capacity of splitting complex oxygen-bearing substances present in the body to produce necessary oxygen.
sulphide.
in it

The water

showed
per

pH

7.2 at

dissolved oxygen, 14.9

c.c.

liter of free

Several investigators studied the influence of abundance or lack

of

oxygen upon different Protozoa. For example, Putter (1905) dem-

onstrated that several ciliates reacted differently

siderable length of time.

when

subjected to

anaerobic condition, some perishing rapidly, others living for a con-

Death is said by Lohner to be brought about by a volume-increase due to accumulation of the waste products. When first starved for a few days and then placed in anaerobic environment, Paramecium and Colpidium died much more rapidly than unstarved individuals. Putter, therefore, supposed that the difference in longevity of aerobic Protozoa in anaerobic conditions was correlated with that of the amount of reserve food material such as protein, glycogen and paraglycogen present in the body. Putter further noticed that

than Spirostomum

Paramecium is less affected by anaerobic condition in a small amount of water, and maintained that

PHYSIOLOGY
the smaller the size of

117
contractile

body and the more elaborate the

vacuole system, the organisms suffer the less the lack of oxygen in the water, since the removal of catabolic products depends upon these
factors.

The variety
a great deal

of habitats

and

results of artificial cultivations of

various Protozoa indicate clearly that the oxygen requirements vary

among

different forms.

Attempts were made

in recent

years to determine the oxygen requirement of Protozoa. The results of the observations are not always convincing. The oxygen consump-

and Amberson oxygen concentration. Specht (1934) found the measurements of the oxygen consumption and carbon dioxide production in Spirostomum ambiguum vary because of the presence of a base produced by the organism. Soule (1925) observed in the cultural tubes of Trypanosoma lewisi and Leishmania tropica, the oxygen contained in about 100 c.c. of air of the test tube is used up in about 12 and 6 days respectively. A single Paramedian caudatum is said to consume in one hour at 21C. from 0.0052 c.c. (Kalmus) to 0.00049 c.c. (Howland and Bernstein) of oxygen. The oxygen consumption of this ciliate in heavy suspensions (3X10 3 to 301 X10 3 in 3 c.c.) and associated bacteria, ranged, according to Gremsbergen and Reynaerts-De Pont (1952), from 1000 to 4000 nM 3 per hour per million individuals at 23.5C. The two observers considered that P. caudatum possesses a typical cytochrome-oxidase system. Amoeba proteus, according to Hulpieu (1930), succumbs slowly when the amount of oxygen in water is less than 0.005 per cent and also in excess, which latter confirms Putter's observation on Spirostomum. According to Clark (1942), a normal Amoeba proteus consumes 1.4 X10~ 3 mm 3 of oxygen per hour, while an enucleated amoeba only 0.2X10 -3 mm 3 He suggests that "the oxygen-carriers concerned with 70 per cent of the normal respiration of an amoeba are related in some way to the presence of the nucleus." In Pelomyxa caroUnensis, the rate of oxygen consumption at 25C. was found by Pace and Belda (1944) to be 0.244+0.028 mm 3 per hour per mm 3 cell substance and does not differ greatly from that of Amoeba proteus and Actinosphaervum eichhorni. The temperature coefficient for the rate of respiration is nearly the same as that in Paramecium, varying from 1.7 at 15-25C. to 2.1 at 25-35C. Pace and Kimura (1946) further note in Pelomyxa caroUnensis that carbohydrate metabolism is greater at higher than at lower temperature and that a cytochrome-cytochrome oxidase system is the mechanism chiefly involved in oxidation of carbohydrate.
tion of

Paramecium

is

said,

according to

Lund

(1918)

(1928), to be fairly constant over a wide range of

118

PROTOZOOLOGY

land (1925),

The Hypermastigina of termites are killed, according to Clevewhen the host animals are kept in an excess of oxygen.

Jahn found that Chilomonas paramedian in bacteria-free cultures in heavily buffered peptone-phosphate media at pH 6.0, required for rapid growth carbon dioxide which apparently brings about a favorable intracellular hydrogen-ion concentration. Respiratory metabolism (Meldrum, 1934; Jahn, 1941).
Excretion and secretion

composed of water, carbon dioxide, and nitrogenous compounds, all of which are soluble, pass out of the body by diffusion through the surface or by means of the contractile
catabolic waste material

The

vacuole

(p. 83).

sidered to possess a molecular

The protoplasm of the Protozoa is generally conmake-up which appears to be similar

among
the
diffuses

those living in various habitats. In the freshwater Protozoa

of which is hypertonic to surrounding water, the water through the body surface and so increases the water content of the body protoplasm as to interfere with its normal function. The contractile vacuole, which is invariably present in all freshwater forms, is the means of getting rid of this excess water from the body.

body

On

the other hand, marine or parasitic Protozoa live in nearly iso-

tonic

media and there

is

no excess

of

water entering the body, hence

the contractile vacuoles are not found in them. Just exactly why nearly all euciliates and suctorians possess the contractile vacuole
regardless of habitat, has not fully been explained. It

the pellicle of the ciliate

is assumed that impermeable to salts and slowly permeable to water (Kitching, 1936) or impermeable to water, salts and prob-

is

ably gases (Frisch, 1937). If this is the case with all ciliates, it is not difficult to understand the universal occurrence of the contractile
vacuole in the ciliates and suctorians. That the elimination of excess amount of water from the body is one of the functions of the contractile vacuole appears to be be-

yond doubt judging from the observations of Zuelzer (1907), Finley (1930) and others, on Amoeba verrucosa which lost gradually its contractile vacuole as sodium chloride was added to the water, losing the organella completely in the seawater concentration and of Yocom (1934) on Paramecium caudatum and Euplotes patella, the contractile vacuoles of which nearly ceased functioning when the animals were placed in 10 per cent sea water. Furthermore, marine amoebae develop contractile vacuoles de novo when they are transplanted to fresh water as in the case of Vahlkampfia calkinsi (Hogue, 1923) and Amoeba biddulphiae (Zuelzer, 1927). Herfs (1922) studied

PHYSIOLOGY
the pulsation of the contractile vacuoles of
fresh

119

water as well as urements:

Per cent

in salt

Paramecium caudatum in water and obtained the following meas-

NaCl

in water

120

PROTOZOOLOGY

through this avenue is not of a large quantity. How much water is produced during the metabolic activity of the organisms is unknown, but it is considered to be a very small amount (Kitching, 1938). The mechanism by which the difference in osmotic pressure can be maintained at the body surface is unknown. It may be, as suggested by Kitching (1934), that the contractile vacuole extrudes water but retains the solutes or some osmotically active substances must be continuously produced within the body. Attempts to detect catabolic products in the contractile vacuole, in the body protoplasm or in the culture fluid, were unsuccessful, because of technical
difficulties.

Weatherby (1927) detected

in

the

Fig. 43. Examples of crystals present in Protozoa, a-e, in Paramecium caudatum (Schewiakoff), (a-d, X1000, e, X2600); f, in Amoeba protetis;
g, in

A. discoides; h-1, in A. dubia (Schaeffer).

spring water in which he kept a number of thoroughly washed Paramecium, urea and ammonia after 30-36 hours and supposed that the urea excreted by the organisms gave rise to ammonia. He found also urea in similar experiments with Spirostomum and Didinium (Weatherby, 1929). Doyle and Harding (1937) found Glaucoma excreting ammonia, and not urea. Carbon dioxide is obviously excreted by the body surface as well as the contractile vacuole. At

present the composition of the fluid in the contractile vacuole

is

not
of

know n. General
7

reference (Weatherby, 1941); permeability of water

in

Protozoa (Belda, 1942; L0vtrup and Pigon, 1951); physiology

1924;

contractile vacuole (Stempell,

Fortner,

1926;

Gaw, 1936;

Kitching, 1938a).

Aside from the soluble forms, there often occur in the protozoan body insoluble substances in the forms of crystals and granules of various kinds. Schewiakoff (1894) first noticed that Paramecium often contained crystals (Fig. 43) composed of calcium phosphate,
starved,

which disappeared completely in 1-2 days when the organisms were and reappeared when food was given. Schewiakoff did not see the extrusion of these crystals, but considered that these crystals

PHYSIOLOGY

121

were first dissolved and excreted by the contractile vacuoles, as they were seen collected around the vacuoles. When exposed to X-irradiation, the symbiotic Chlorella of

Paramecium bursaria disappear

gradually and crystals appear and persist in the cytoplasm of the

ciliate (Wichterman, 1948a). These crystals varying in size from a few to 12m, are found mainly in the posterior region of the body. Wichterman notes that the appearance or disappearance of crystals seems to be correlated with the absence or presence of symbiotic Chlorella and with the holozoic or holophytic (by the alga) nutrition

of the organism.

In Amoeba proteus, Schubotz (1905) noted crystals of calcium phosphate which were bipyramidal or rhombic in form, were doubly refractile and measured about 2-5m in length. In three species of Amoeba, Schaeffer (1920) points out the different shape, number and dimensions of the crystals. Thus in Amoeba proteus, they are truncate bipyramids, rarely flat plates, up to 4.5m long; in A. discoides, abun-

up to 2.5m long; and in .4. dubia, variously shaped (4 kinds), few, but large, up to 10m, 12m, 30m long (Fig. 43). Bipyramidal or plate-like crystals are especially abundant in
dant, truncate bipyramids,
all times (Kudo, 1951); the crystals of P. remain the same during the starvation of the organism (Andresen and Holter, 1945; Holter, 1950). The crystals present in Protozoa appear to be of varied chemical nature. Luce and Pohl (1935) noticed that at certain times amoebae in culture are clear and contain relatively a few crystals but, as the culture grows older and the water becomes more neutral, the crystals become abundant and the organisms become opaque in transmitted light. These crystals are tubular and six-sided, and vary in length from 0.5 to 3.5m- They considered the crystals were composed of calcium chlorophosphate. Mast and Doyle (1935), on the

Pelom.yxa illinoisensis at

carolinensis

other hand, noted in

like

Amoeba proteus two kinds of crystals, plateand bipyramidal, which vary in size up to 7m in length and which are suspended in alkaline fluid to viscous vacuoles. These two

authors believed that the plate-like crystals are probably leucine, while the bipyramidal crystals consist of a magnesium salt of a substituted glycine. Other crystals are said to be

composed

of urate,

carbonate, oxalate, etc.

Another catabolic product is the haemozoin (melanin) grains which occur in many haemosporidians and which appear to be composed of a derivative of the haemoglobin of the infected erythrocyte (p. 605). In certain Radiolaria, there occurs a brownish amorphous mass which is considered as catabolic waste material and, in Foram-

122
inifera, the

PROTOZOOLOGY
cytoplasm
is

frequently loaded with masses of brown

granules which appear also to be catabolic waste and are extruded

from the body periodically. While intracellular secretions are usually difficult to recognize, because the majority remain in fluid form except those which produce endoskeletal structures occurring in Foraminifera, Heliozoa,
Radiolaria, certain parasitic ciliates, etc., the extracellular secretions
are easily recognizable as loricae, shells, envelopes, stalks, collars,

mucous substance,

etc.

Furthermore,

many

Protozoa secrete, as was

stated before, certain substances through the pseudopodia, tentacles

or trichocysts which possess paralyzing effect

upon the

preys.

Movements
Protozoa move about by means of the pseudopodia, flagella, or cilia, which may be combined with internal contractile organellae. Movement by pseudopodia. Amoeboid movements have long been studied by numerous observers. The first attempt to explain the movement was made by Berthold (1886), who held that the difference in the surface tension was the cause of amoeboid movements, which view was supported by the observations and experiments of Butschli (1894) and Rhumbler (1898). According to this view, when an amoeba forms a pseudopodium, there probably occurs a diminution of the surface tension of the cytoplasm at that point, due to certain internal changes which are continuously going on within the

body and possibly due

to external causes,

and the internal pressure

of

the cytoplasm will then cause the streaming of the cytoplasm. This

pseudopodium which becomes attached and an increase in tension of the plasma-membrane draws up the posterior end of the amoeba, thus bringing about
results in the formation of a

to the substratum

movement of the whole body. Jennings (1904) found that the movement of Amoeba verrucosa (Fig. 44, a) could not be explained by the surface tension theory, since he observed "in an advancing amoeba substance flows forward on the upper surface, rolls over at the anterior edge, coming in contact with the substratum, then remains quiet until the body of the amoeba has passed over it. It then moves upward at the
the
posterior end,

and forward again on the upper

surface, continuing

in rotation as long as the

amoeba continues to progress." Thus Amoeba verrucosa may be compared with an elastic sac filled with fluid. Dellinger (1906) studied the movement of Amoeba proteus, A.
and Difflugia
spiralis.

verrucosa

that the

amoeba

(Fig. 45)

Studying in side view, he found extends a pseudopod, "swings it about,

PHYSIOLOGY

123

brings it into the line of advance, and attaches it" to the substratum and that there is then a concentration of the substance back of this point and a flow of the substance toward the anterior end. Dellinger held thus that "the movements of amoebae are due to the presence

Fig. 44. a, diagram showing the movement of Amoeba verrucosa in side view (Jennings) b, a marine limax-amoeba in locomotion (Pantin from Reichenow). ac, area of conversion; cet, contracting ectoplasmic tube; fe, fluid ectoplasm; ge, gelated ectoplasm.

which was said to be located in the endoplasm as a coarse reticulum. Wilber (1946) pointed out that Pelomyxa carolinensis carries on a similar movement at times.
of a contractile substance,"

Fig. 45. Outline sketches of photomicrographs of Amoeba protexis during locomotion, as viewed from side (Dellinger).

In the face of advancement of our knowledge on the nature of protoplasm, Rhumbler (1910) realized the difficulties of the surface tension theory and later suggested that the conversion of the ectoplasm to endoplasm and vice versa were the cause of the cytoplasmic

124

PROTOZOOLOGY
Hyman
(1917).

movements, which was much extended by

considered that:
(1)

Hyman

a gradient in susceptibility to potassium cyanide exists in each pseudopodium, being the greatest at the distal end,

and the most recent pseudopodium, the most susceptible; (2) the susceptibility gradient (or metabolic gradient) arises in the amoebae before the pseudopodium appears and hence the metabolic change which produces increased susceptibility, is the primary cause of pseudopodium formation; and (3) since the surface is in a state of gelation, amoeboid movement must be due to alterations of the colloidal state. Solation, which is brought about by the metabolic change, is regarded as the cause of the extension of a pseudopodium, and gelation, of the withdrawal of pseudopodia and of active contraction. Schaeffer (1920) mentioned the importance of the surface layer which is a true surface tension film, the ectoplasm, and the streaming of endoplasm in the amoeboid movement. Pantin (1923) studied a marine limax-type amoeba (Fig. 44, 6) and came to recognize acid secretion and absorption of water at the place where the pseudopodium was formed. This results in swelling of the cytoplasm and the pseudopodium is formed. Because of the acidity, the surface tension increases and to lower or reduce this, concentration of substances in the "wall" of the pseudopodium follows. This
leads to the formation of a gelatinous ectoplasmic tube which, as the

pseudopodium extends, moves toward the posterior region where the acid condition is lost, gives up water and contracts finally becoming transformed into endoplasm near the posterior end. The contraction
of the ectoplasmic

tube forces the endoplasmic streaming to the

front.

This observation is in agreement with that of Mast (1923, 1926, who after a series of carefully conducted observations on Amoeba proteus came to hold that the amoeboid movement is brought about by "four primary processes; namely, attachment to
1931) the substratum, gelation of plasmasol at the anterior end, solation of
at the posterior

plasmagel at the posterior end and the contraction of the plasmagel end" (Fig. 46). As to how these processes work, Mast states: "The gelation of the plasmasol at the anterior end ex-

tends ordinarily the plasmagel tube forward as rapidly as it is broken down at the posterior end by solation and the contraction of the

plasmagel tube at the posterior end drives the plasmasol forward. The plasmagel tube is sometimes open at the anterior end and the plasmasol extends forward and comes in contact with the plasmalemma at this end (Fig. 47, a), but at other times it is closed by a thin sheet of gel which prevents the plasmasol from reaching the

PHYSIOLOGY

12.5

ot

Fig. 46. Diagram of Amoeba proteus, showing the solation the cytoplasm during amoeboid

and gelation
pg plasma-

movement

(Mast),

c,

tractile vacuole; f food vacuole; he, hyaline cap; n, nucleus; gel; pgs, plasmagel sheet; pi, plasmalemma; ps, plasmasol

crystal: cv con-

126

PROTOZOOLOGY
(6).

anterior end

able periods, being built

This gel sheet at times persists intact for considerup by gelation as rapidly as it is broken

down by
it.

owing to the pressure of the plasmagel against breaks periodically at various places. Sometimes the breaks are small and only a few granules of plasmasol pass through and these gelate immediately and close the openings (d). At other
stretching,
it

Usually

times the breaks are large and plasmasol streams through, filling the hyaline cap (c), after which the sol adjoining the plasmalemma gel-

Fig. 47. Diagrams of varied cytoplasmic movements at the tip of a pseudopodium in Amoeba proteus (Mast), g, plasmagel; he, hyaline cap; hi, hyaline layer; pi, plasmalemma; s, plasmasol.

ates forming a

new

gel sheet.

An amoeba

is

a turgid system, and the

under continuous tension. The plasmagel is elastic and, consequently, is pushed out at the region where its elasticity is weakest and this results in pseudopodial formation. When an amoeba is elongated and undergoing movement, the elastic strength of the plasmagel is the highest at its sides, lowest at the anterior end and intermediate at the posterior end, which results in continuity of the elongated form and in extension of the anterior end. If pressure is brought against the anterior end, the direction of streaming of plasmasol is immediately reversed, and a new hyaline cap is formed at the posterior end which is thus changed into a new anterior end." The rate of amoeboid locomotion appears to be influenced by enplasmagel
is

vironmental factors such as pH, osmotic pressure, salt concentration, substratum, temperature, etc. (Mast and Prosser, 1932). Flagellar movement. The flagellar movement is in a few instances observable as in Peranema, but in most cases it is very difficult to observe in life. Since there is difference in the number, location, size, and probably structure (p. 53) of flagella occurring in Protozoa, it is supposed that there are varieties of flagellar movements. The first explanation was advanced by Biitschli, who observed that the flagel-

PHYSIOLOGY
lum undergoes a
sure
is

127
in so doing, a pres-

series of lateral

movements and,
its

exerted on the water at right angles to

surface. This pres-

sure can be resolved into

two

forces: one directed parallel,

and the

other at right angles, to the main

body

axis.

The former

will drive

the organism forward, while the latter will tend to rotate the animal

on

its own axis. Gray (1928), who gave an

excellent account of the

movement

of

flagella,

points out that "in order to produce propulsion there

must

be a force which is always applied to the water in the same direction and which is independent of the phase of lateral movement. There can be little doubt that this condition is satisfied in flagellated organisms not because each particle of the flagellum is moving laterally to and fro, but by the transmission of the waves from one end of the flagellum to the other, and because the direction of the transmission is always the same. A stationary wave, as apparently contemplated by Biitschli, could not effect propulsion since the forces acting on the water are equal and opposite during the two phases of the movement. If however the waves are being transmitted in one direction only, definite propulsive forces are present which always act in a
direction opposite to that of the waves."

Because of the nature of the flagellar movement, the actual procnot been observed. Verworn observed long ago that in Peranema trichophorum the undulation of the distal portion of flagellum is accompanied by a slow forward movement, while undulation along the entire length is followed by a rapid forward movement. Krijgsman (1925) studied the movements of the long flagellum of Monas sp. (Fig. 48) which he found in soil cultures, under the darkfield microscope and stated: (1) when the organism moves forward with the maximum speed, the flagellum starting from c 1, with the wave beginning at the base, stretches back (c 1-6), and then waves back (d, e), which brings about the forward movement. Another type is one in which the flagellum bends back beginning at its base (/) until it coincides with the body axis, and in its effective stroke waves back as a more or less rigid structure (g) (2) when the organism moves forward with moderate speed, the tip of the flagellum passes through 45 or less (h-j) (3) when the animal moves backward, the flagellum undergoes undulation which begins at its base (k-o) (4) when the animal moves to one side, the flagellum becomes bent at right angles to the body and undulation passse along it from its base to tip (p); and (5) when the organism undergoes a slight lateral movement, only the distal end of the flagellum undulates (q). Ciliary movement. The cilia are the locomotor organella present
ess has often
;

128

PROTOZOOLOGY
in the ciliates

permanently

and vary

in size

different species. Just as flagellates

and distribution among show various types of move-

swim

ments, so do the ciliates, though nearly all free-swimming forms in a spiral path (Bullington, 1925, 1930). Individual cilium on a

Fig.

48.

Diagrams

illustrating

flagellar

movements

of

Monas

sp.

(Krijgsman). a-g, rapid forward movement (a, b, optical image of the movement in front and side view; c, preparatory and d, e, effective stroke; f, preparatory and g, effective stroke); h-j, moderate forward movement (h, optical image; i, preparatory and j, effective stroke); k-o, undulatory movement of the flagellum in backward movement; p, lateral movement; q, turning movement.

PHYSIOLOGY
progressing ciliate bends throughout
so that the organism tends to
its

129

length and strikes the water

move

in a direction opposite to that of

the effective beat, while the water

(Fig. 49, a-d).

moves in the direction of the beat In the Protociliata and the majority of holotrichous

and heterotrichous ciliates, the cilia are arranged in longitudinal, or oblique rows and it is clearly noticeable that the cilia are not beating in the same phase, although they are moving at the same rate. A

/" "^

j
1

'5

W/^mr^ll
Fig.
49.

^gc
movements (Verworn). a-d,
and
c,

Diagrams

illustrating

ciliary

movement

of a marginal cilium of Urostyla grandis (a, preparatory

b, effective stroke,

resulting in rapid

movement;
;

preparatory, and d,

effective stroke, bringing

about moderate speed)

e,

metachronous move-

ments of

cilia in

a longitudinal row.
e) in

cilium (Fig. 49,

behind

is slightly in advance of the cilium behind the one just in front of it, thus the cilia on the same longitudinal row beat metachronously. On the other hand, the cilia on the same transverse row beat synchronously, the condition clearly being recognizable on Opalina among others, which is much like the waves passing over a wheat field on a windy
it

a single row

and

slightly

day.

The organized movements of cilia, cirri, membranellae and unmembranes are probably controlled by the neuromotor system (p. 63) which appears to be conductile as judged by the
dulating
results of micro-dissection
;

experiments of Taylor

(p. 65).

Ciliary

movement (Gray, 1928) spiral movement of ciliates (Bullington, 1925, 1930); movement of Paramecium (Dembowski, 1923, 1929a)
and
of Spirostomum (Blattner, 1926). The Protozoa which possess myonemes

are able to

move by

con-

130
traction of the
secretion of

PROTOZOOLOGY
body or of the stalk, and others combine this with the mucous substance as is found in Haemogregarina and

Gregarinida.
Irritability

Under natural conditions, the Protozoa do not behave always in same manner, because several stimuli act upon them usually in combination and predominating stimulus or stimuli vary under different circumstances. Many investigators have, up to the present
the
time, studied the reactions of various Protozoa to external stimula-

which is beyond the scope of the present work. Here one or two examples in connection with the reactions to each of the various stimuli only will be mentioned. Of various responses expressed by a protozoan against a stimulus such as
tions, full discussion of

changes in body form, movement, structure, behavior, etc., the movement is the most clearly recognizable one and, therefore, freeswimming forms, particularly ciliates, have been the favorite objects of study. We consider the reaction to a stimulus in protozoans as the movement response, and this appears in one of the two directions: namely, toward, or away from, the source of the stimulus. Here we speak of positive or negative reaction. In forms such as
face

Amoeba, the external stimulation is first received by the body surand then by the whole protoplasmic body. In flagellated or
of ciliates are

ciliated Protozoa, the flagella or cilia act in part sensory; in fact in a

number

found non-vibratile

cilia

which appear to be
of forms, there

sensory in function. In a comparatively small

vacuoles, etc.

number

are sensory organellae such as stigma, ocellus, statocysts, concretion

In general, the reaction of a protozoan to any external stimulus depends upon its intensity so that a certain chemical substance may bring about entirely opposite reactions on the part of the protozoans in different concentrations and, even under identical conditions,
different individuals of a given species
tability (Jennings, 1906;

may
in

react differently. Irri-

Mast, 1941);

Spirostomum (Blattner,

1926).

Reaction to mechanical stimuli. One of the most

common
is

stimuli

a protozoan would encounter in the natural habitat

that which

comes from contact with a solid object. When an amoeba which Jennings observed, came in contact with the end of a dead algal filament at the middle of its anterior surface (Fig. 50, a), the amoeboid

movements proceeded on both

sides of the filament (6),

soon motion ceased on one

side, while it

but continued on the other, and

PHYSIOLOGY

131

the organism avoided the obstacle by reversing a part of the current and flowing in another direction (c) When an amoeba is stimulated mechanically by the tip of a glass rod (rf), it turns away from the side touched, by changing endoplasmic streaming and forming new pseudopodia (e). Positive reactions are also often noted, when a suspended amoeba (/) comes in contact with a solid surface with the tip of a pseudopodium, the latter adheres to it by spreading out (g). Streaming of the cytoplasm follows and it becomes a creeping form
.

Fig. 50. Reactions of

amoebae

to mechanical stimuli (Jennings), a-c,

an amoeba avoiding an obstacle;

d, e, negative reaction to mechanical stimulation; f-h, positive reaction of a floating amoeba.

(h).

Positive reactions toward solid bodies account of course for the

ingestion of food particles.

In Paramecium, according to Jennings, the anterior end

sensitive

is

more

than any other parts, and while swimming, if it comes in contact with a solid object, the response may be either negative or positive. In the former case, avoiding movement (Fig. 51, c) follows and in the latter case, the organism rests with its anterior end or the whole side in direct contact with the object, in which position it ingests food particles through the cytostome. Reaction to gravity. The reaction to gravity varies among different Protozoa, according to body organization, locomotor organelle, etc. Amoebae, Testacea and others which are usually found attached to the bottom of the container, react as a rule positively

132

PROTOZOOLOGY

toward gravity, while others manifest negative reaction as in the Paramecium (Jensen; Jennings), which explains in part why Paramecium in a culture jar are found just below the surface film in mass, although the vertical movement of P. caudatum is undoubtedly influenced by various factors (Koehler, 1922, 1930; Dembowski, 1923, 1929, 1929a; Merton, 1935). Reaction to current. Free-swimming Protozoa appear to move
case of
or orientate themselves against the current of water. In the case of

PHYSIOLOGY

133

area of a drop of 0.02 per cent acetic acid introduced to the preparation (Fig. 51, a); and if stronger acid is used, the organisms collect

about its periphery where the acid is diluted by the surrounding water (b) The reaction to chemical stimuli is probably of the greatest importance for the existence of Protozoa, since it leads them to proper food substances, the ingestion of which is the foundation of
.

metabolic activities. In the case of parasitic Protozoa, possibly the reaction to chemical stimuli results in their finding specific host animals and their distribution in different organs and tissues within the
host body. Recent investigations tend to indicate that chemotaxis plays an important role in the sexual reproduction in Protozoa.
in Peranema (Chen, 1950). Reaction to light stimuli. Most Protozoa seem to be indifferent to the ordinary light, but when the light intensity is suddenly increased, there is usually a negative reaction. Verworn saw the di-

Chemotaxis

rection of movements of an amoeba reversed when its anterior end was subjected to a sudden illumination; Rhumbler observed that an amoeba, which was in the act of feeding, stopped feeding when it was subjected to strong light. According to Mast, Amoeba proteus ceases to move when suddenly strongly illuminated, but continues to move if the increase in intensity is gradual and if the illumination remains constant, the amoeba begins to move. Pelomyxa carolinensis reacts negatively to light (Kudo, 1946). The positive reaction to light is most clearly shown in stigma-

bearing Mastigophora, as

is

well observable in a jar containing

collect at the place

Euglena, Phacus,

etc., in

which the organisms

where the light is strongest. If the light is excluded completely, the organisms become scattered throughout the container, inactive and sometimes encyst, although the mixotrophic forms would continue activities by saprozoic method. The positive reaction to light by chromatophore-bearing forms enables them to find places in the water where photosynthesis can be carried on to the maximum
degree.
All Protozoa seem to be more sensitive to ultraviolet rays. Inman found that amoeba shows a greater reaction to the rays than others and Hertel observed that Paramecium which was indifferent to an ordinary light, showed an immediate response (negative reaction) to the rays. MacDougall brought about mutations in Chilodonella by means of these rays (p. 229). Horvath (1950) exposed Kahlia simplex to ultraviolet rays and destroyed the micronucleus. The emicronucleate individuals lived and showed a greater vitality than nor-

mal individuals, as judged by the division rate at 34C. Mazia and

134

PROTOZOOLOGY
Amoeba
of the

Hirshfield (1951) subjected

proteus to ultraviolet radiation

whole and nucleated half amoebae delays division immediately following exposure; later progeny of the irradiated amoebae have a normal division rate; amputation of half of the cytoplasm greatly increases the radiation sensitivity as measured by delayed division or by the dose required for permanent inhibition of division (sterilization dose) individuals that have received this dose may survive for 20-30 days; and the survival time of an enucleate fragment is very much reduced by small (200-500 ergs/sq. mm) doses. The two workers consider that the overall radiation effect may have both nuclear and cytoplasmic components. By exposing Pelomyxa carolinensis to 2537 A ultraviolet irradiation, Wilber and Slane (1951) found the effects variable; however, all recovered from a two minutes' exposure, none survived a 10-minute exposure, and 70 per cent of fat were released after two minutes'
;

and noticed that irradiation

exposure.

Zuelzer (1905) found the effect of radium rays upon various Pro-

tozoa vary; in
first effect of

all cases, a long exposure was fatal to Protozoa, the exposure being shown by accelerated movement. Hal-

berstaedter and Luntz (1929, 1930) studied injuries and death of

in culture

Eudorina elegans by exposure to radium rays. Entamoeba histolytica when subjected to radium rays, Nasset and Kofoid (1928)

noticed the following changes: the division rate rose two to four

times by the exposure, which effect continued for not more than 24

hours after the removal of the radium and was followed by a retardation of the rate; radium exposure produced changes in nuclear structure, increase in size, enucleation or autotomy, which were more striking when a larger amount of radium was used for a short time than a smaller amount acting on for a long time; and the effects
persisted for four to six days after the removal of the radium and then the culture gradually returned to normalcy. Halberstaedter (1914) reported that when exposed to Beta rays, Trypanosoma
brucei lost its infectivity,

though remained

alive.

Halberstaedter (1938) exposed Trypanosoma gambiense to X-rays and found that 12,000r rendered the organisms not infectious for mice, while 600,000r was needed to kill the flagellates. Emmett
(1950) exposed T. cruzi to X-rays and noticed that dosages between 51,000r and 100,000r were necessary to destroy the infectivity of this

trypanosome; the cultures, after exposure to 100,000r, appeared to be thriving up to three months; and the effects of exposure were not
passed on to

new

generations.

When Paramecium

bursaria were exposed to X-rays,

Wichterman

PHYSIOLOGY

135

(1948) noted: dosages higher than 100,0Q0r retard the locomotion of the ciliate; none survives 700,000r; the symbiotic Chlorella is destroyed by exposure to 300,000-000,000?' ; irradiation inhibits di-

normal division rate and mating types are not destroyed, though minor changes occur. In Pelomyxa carolinensis, Daniels (1951) observed: the median lethal dose of X-rays is 96,000r; with dosages 15,000-140,000r, the first plasmotomy is greatly delayed and the second plasmotomy is also somewhat delayed, but later plasmotomies show complete recovery; X-irradiation does not change the type of plasmotomy; and in individuals formed by plasmogamy
division temporarily, but the animals recover
after certain length of time;
of X-irradiated halves to non-irradiated halves, the nuclei divide

simultaneously as in a normal individual. Reaction to temperature stimuli. As was stated before, there seems to be an optimum temperature range for each protozoan, although it can withstand temperatures which are lower or higher

than that range. As a general

turn in

rule,

the higher the temperature, the

greater the metabolic activities,

and the latter condition results in a more rapid growth and more frequent reproduction. It has

been suggested that change to different phases in the life-cycle of a protozoan in association with the seasonal change may be largely due to temperature changes of the environment. In the case of
parasitic Protozoa

which inhabit two hosts: warm-blooded and cold-

blooded animals, such as Plasmodium and Leishmania, the difference in body temperature of host animals may bring about specific stages
in their

development. Reaction to electrical stimuli.

Since

Verworn's experiments,

several investigators studied the effects of electric current which

action to the anode

Amoeba shows negative reand moves toward the cathode either by reversing the cytoplasmic streaming (Verworn) or by turning around the body (Jennings). The free-swimming ciliates move mostly toward
is

passed through Protozoa in water.

the cathode, but a few

or

may take a transverse position (Spirostomum)

swim to the anode (Paramecium, Stentor, etc.). Of flagellates, Verworn noticed that Trachelomonas and Peridinium moved to the cathode, while Chilomonas, Cryptomonas, and Polytomella, swam to the anode. When Paramecium caudatum was exposed to a highfrequency electrostatic or electromagnetic field, Kahler, Chalkley and Voegtlin (1929) found the effect was primarily caused by a temperature increase in the organism.

By

subjecting Pelomyxa carolin-

ensis to a direct current electric field, Daniel

that the time required for the rupture of the

and May (1950) noted body in a given current

136

PROTOZOOLOGY

is directly correlated with the size of the organism and that calcium increases the time required for rupture at a fixed body size

density

and current density, but does not

of

alter the size effect. Galvanotaxis Oxytricha (Luntz, 1935), of Arcella (Miller, 1932).

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(1923) Zur Physiologie der saprophytischer Flagellaten. Beitr. allg. Bot., 2:88. (1928) Physiologische Untersuchungen an Paramecium bursaria,

Arch. Protist., 64:289.

(1937) Beitrage zur Physiologie der saprophytischer Algen und Flagellaten. I. Planta, 26:631. (1937a) Algenreinkulturen. Arch. Protist., 88:143. and Hovasse, R. (1948) The loss of chromatophores in Euglena gracilis. The New Phytologist., 47:52. Putter, A.: (1905) Die Atmung der Protozoen. Ztschr. allg. Physiol., 5:566. (1908) Methoden zur Forschung des Lebens der Protisten. Tigerstedt's Handb. physiol. Methodik., 1:1. Ray, D. L. (1951) Agglutination of bacteria: a feeding method in the soil ameba Hartmannella sp. Jour. Exp. Zool., 118:443. Reichenow, E.: (1909) Untersuchungen an Haematococcus pluvialis, etc. Berlin. Sitz.-Ber. Ges. naturf. Freunde, p. 85. Rhumbler, L. (1910) Die verschiedenartigen Nahrungsaufnahmen bei Amoeben als Folge verschiedener Colloidalzustande ihrer Oberflachen. Arch. Entw. Organ., 30:194. Richards, O. W. (1941) The growth of the Protozoa. In: Calkins and Summers (1941). Robertson, T. B.: (1921) Experimental studies on cellular multiplication. I. Biochem. J., 15:595. (1921a) II. Ibid., 15:612. (1924) The nature of the factors which determine the duration of the period of lag in cultures of Infusoria. Australian J. Exper. Biol, 1:105. (1924a) The influence of washing upon the multiplication of isolated Infusoria and upon the allelocatalytic effect in cultures initially containing two Infusoria. Ibid., 1:151. (1924b) Allelocatalytic effect in cultures of Colpidium in hay infusion and in synthetic media. Biochem. J., 18:1240. (1927) On some conditions affecting the viability of Infusoria

PHYSIOLOGY
and the occurrence
per. Biol.. 4:1.

143

of allelocatalysis therein. Australian J.

Ex-

(1925) Ueber die Axopodien der Heliozoa und die Greiftentakel der Ephelotidae. Arch. Protist., 52:207. and Levinsohn, L. (1926) Die Oxydasen und Peroxydasen bei Protozoen. Ibid., 56: 145. Rumjantzew, A. and Wermel, E.: (1925) Untersuchungen ueber den Protoplasmabau, etc. Arch. Protist., 52:217. Sassuchin, D. N.: (1935) Zum Studium der Protisten- und Bakterienkerne. I. Ibid., 84:186. Schaeffer, A. A.: (1920) Amoeboid movement, Princeton. Schewiakoff, W. (1894) Ueber die Natur der sogennannten Exkretkorner der Infusorien. Ztschr. wiss. Zool., 57:32. Schulze, K. L. (1951) Experimentelle Untersuchungen ueber die Chlorellen-symbiose bei Ciliaten. Biol. Gen., Vienna, 19:281. Seaman, G. R. and Houlihan, R. K. (1951) Enzyme systems in Tetrahymena geleii S. II. J. Cell. Comp. Physiol., 37:309. Shapiro, N. N.: (1927) The cycle of hydrogen-ion concentration in the food vacuoles of Paramecium, Vorticella, and Stylonychia. Tr. Am. Micr. Soc, 46:45. Soule, M. H.: (1925) Respiration of Trypanosoma lewisi and Leishmania tropica. J. Infect. Dis., 36:1245. Specht, H. (1934) Aerobic respiration in Spirostomum ambiguum, etc. J. Cell Comp. Physiol., 5:319. Stempell, W. (1924) Weitere Beitrage zur Physiologie der pulsierenden Vakuole von Paramecium. I. Arch. Protist., 48:342. Stolc, A.: (1900) Beobachtungen und Versuche ueber die Verdauung und Bildung der Kohlenhydrate bei einen amoebenartigen Organismen, Pelomyxa palustris. Ztschr. wiss. Zool., 68:

Roskin, G.

625.

Tanabe, M. and Komada, K. (1932) On the cultivation

:

of

Balan-

tidium colt. Keijo J. Med., 3:385. Taylor, C. V.: (1923) The contractile vacuole in Euplotes, etc. J. Exper. Zool., 37:259. Trager, W. (1932) A cellulase from the symbiotic intestinal flagellates of termites, etc. Biochem. J., 26: 1762. Turner, J. P.: (1940) Cytoplasmic inclusions in the ciliate Tillina canalifera. Arch. Protist., 93:255. Veley, Lilian J.: (1905) A further contribution to the study of Pelomyxa palustris. J. Linn. Soc. Zool., 29:374. Verworn, M.: (1889) Psycho-physiologische Protisten-Studien. Jena. (1903) Allgemeine Physiologie. 4 ed. Jena. Weatherby, J. H. (1927) The function of the contractile vacuole in Paramecium caudatum. Biol. Bull., 52:208. (1929) Excretion of nitrogenous substances in Protozoa. Physiol. Zool., 2:375. (1941) The contractile vacuole. In: Calkins and Summers
: :

(1941).

144

PROTOZOOLOGY
:

(1934) Die Celluloseverdauung bei den Ciliaten des Wiederkauermagens. Arch. Protist., 82:169. Whipple, G. C: (1927) The microscopy of drinking water. 4th ed. New York. Wichterman, R. (1948) The biological effects of X-rays on mating types and conjugation of Paramecium, bursaria. Biol. Bull., 94:
:

Weineck, E.

113.

(1948a) The presence of optically active crystals in Paramecium bursaria and their relationship to symbiosis. Anat. Rec, 101:97.

Wilber, C. G.: (1945) Origin and function of the protoplasmic constituents in Pelomyxa carolinensis. Biol. Bull., 88:207.

(1945a)

etc. Tr.

(1946) Notes on locomotion in Pelomyxa carolinensis. Ibid., 65:318. and Slane, Gertrude M.: (1951) The effect of ultraviolet light on the protoplasm in Pelomyxa carolinensis. Ibid., 70:265. Yocom, H. B.: (1934) Observations on the experimental adaptation of certain freshwater ciliates to sea water. Biol. Bull., 67:273. Zeuthen, E. (1948) Reduced weight and volume during starvation of the amoeba, etc. C. R. Lab. Carlesberg, Ser. Chim., 26:267. Zingher, J. A.: (1934) Beobachtungen an Fetteinschliissen bei einigen Protozoen. Arch. Protist., 82:57. Zuelzer, M.: (1905) Ueber die Einwirkung der Radiumstrahlen auf Protozoen. Ibid., 5:358. (1907) Ueber den Einfiuss des Meerwassers auf die pulsierende Vacuole. Berlin. Sitz.-Ber. Ges. naturf. Freunde, p. 90. (1927) Ueber Amoeba biddulphiae, etc. Arch. Protist., 57:
:

The composition of the Am. Micr. Soc, 64:289.

refractive bodies in rhizopod,

247.

Zumstein, H.: (1900) Zur Morphologie und Physiologie der Euglena gracilis. Pringsheims Jahrb. wiss. Botanik., 34:149.

Chapter

Reproduction
reproduction THE modegroups, although
of

in
it

Protozoa
is

is

highly variable

different

primarily a

cell division.

among The

reproduction

is

initiated

by the nuclear
first.

division in nearly all cases,

which

will therefore

be considered

Nuclear division

Between a simple

direct division on the one

is

plicated indirect division which

hand and a comcomparable with the typical

all

metazoan mitosis on the other hand,

occur.

types of nuclear division

Direct nuclear division. Although not so widely found as it was thought to be in former years, amitosis occurs normally and regularly in many forms. While the micronuclear division of the Ciliophora is mitotic (p. 165), the macronuclear division is invariably amitosis. The sole exception to this general statement appears to be the so-called promitosis reported by Ivanic (1938) in the macro-

nucleus in the "Vermehrungsruhe" stage of Chilodenella uncinata in

which chromosomes and spindle-fibers were observed. In Paramecium caudatum (Fig. 52), the micronucleus initiates the division by mitosis and the macronucleus elongates itself without any visible changes in its internal structure. The elongated nucleus becomes constricted through the middle and two daughter nuclei are produced.

assumed that the nuclear components undergo solation during formed particles of nucleus which are stationary in the resting stage manifest a very active Brownian movement. Furthermore, in some cases the nuclear components may undergo phase reversal, that is to say, the chromatin granules which are disIt is

division, since the

persed phase in the non-staining fluid dispersion

ing nucleus,

medium

in the rest-

become dispersion medium

in

which the

latter is sus-

pended as dispersed phase. By using Feulgen's nucleal reaction, Reichenow (1928) demonstrated this reversal phenomenon in the division of the macronucleus of Chilodonella cucullulus (Fig. 53). The macronucleus becomes at the time of its division somewhat enlarged and its chromatin granules are more deeply stained than before. But chromosomes which characterize the mitotic division are entirely absent, although in a few forms in which mating types occur, the type difference and certain other characters, according to
145

146

PROTOZOOLOGY

Sonneborn and Kimball, appear to be under control of genie constituents of the macronucleus. Since the number of chromatin granules appear approximately the same in the macronuclei of different generations of a given species, the reduced number of chromatin gran-

Fig. 52. Nuclear and cytoplasmic division of Paramecium caudatum as seen in stained smears, X260 (Kudo).

ules

must be restored sometime before the next

is

division takes place.

"each granule elongates and divides into two parts, thus doubling the number of chromomeres." Reichenow (1928) found that in Chilodonella cucullulus the lightly Feulgen positive endosome appeared to form chromatin granules and Kudo (1936) maintained that the large chromatin spherules of
of the opinion that

Calkins (1926)

REPRODUCTION
spherules in their alveoli (Fig. 3).

147

the macronucleus of Nyctotherus ovalis probably produce smaller

When

the macronucleus
etc.,

is

elongated as in Spirostomum, Stentor.

of the elongated

Euplotes,

the nucleus becomes condensed into a rounded form

prior to its division.

During the "shortening period"

macronuclei prior to division, there appear 1-3 characteristic zones which have been called by various names, such as nuclear clefts, reconstruction bands, reorganization bands, etc. In Euplotes patella

Fig. 53. The solation of chromatin during the macronuclear division of Chilodonella cucullulus, as demonstrated by Feulgen's nucleal reaction,

Xl800(Reichenow).

Turner (1930) observed prior to division of the macronucleus a reorganization band consisting of a faintly staining zone ("reconstruction plane") and a deeply staining zone ("solution plane"), appears at each end of the nucleus (Fig. 54, a) and as each moves toward the center, a more chromatinic area is left behind (b-d). The two bands finally meet in the center and the nucleus assumes an ovoid form. This is followed by a simple division into two. In the T-shaped macronucleus of E. woodruffi, according to Pierson (1943), a reorganization band appears first in the right arm and the posterior tip of the stem of the nucleus. When the anterior band reaches the junction of the arm and stem, it splits into two, one part
(E. eury stomas)
,

148

PROTOZOOLOGY

ing

moving along the left arm to its tip, and the other entering and passdown the stem to join the posterior band. According to Summers
(1935) a process similar to that of E. eurystomus occurs in Diophrys

appendiculata and Stylonychia pustulata; but in Aspidisca lynceus

band appears first near the middle region macronucleus (6), divides into two and each moves toward an end, leaving between them a greater chromatinic content of the reticulum (c-i). Summers suggested that "the reorganization bands are local regions of karyolysis and resynthesis of macronuclear materials with the possibility of an elimination of physically or
(Fig. 55) a reorganization
of the

possibly chemically modified nonstaining substances into the cyto-

plasm." Weisz (1950a) finds that the nodes of the moniliform macro-

Fig. 54. Macronuclear reorganization before division in Euplotes eurystomus, X240 (Turner), a, reorganization band appearing at a tip of the macronucleus; b-d, later stages.

nucleus of Stentor coeruleus contain different concentration of thymonucleic acid which

is

correlated with morphogenetic activity of indi-

vidual nodes, and that fusion of ill-staining nodes results in a return

of strong affinity to

methyl green.

It appears, therefore, concentra-

tion of

bandform

or moniliform macronucleus prior to division

may

serve to recover morphogenetic potential prior to division.

In a small number of

ciliates,

the macronucleus

is

distributed as

small bodies throughout the cytoplasm. In Urostyla grandis, the

macronuclear material

is

lodged in 100 or more small bodies scatall

tered in the cytoplasm. Prior to fission,

macronuclear bodies fuse

with one another and form one macronucleus which then divides three times into eight and the latter are evenly distributed between the two daughter individuals, followed by divisions until the number reaches 100 or more (Raabe, 1947). On the other hand, in Dileptus

REPRODUCTION
anser (Fig. 310,
c),

149

and with the majority

"each granule divides where it happens to be of granules both halves remain in one daugh-

ter cell after division" (Calkins).

Hayes noticed a

similar division,

but at the time of simultaneous division prior to cell division, each macronucleus becomes elongated and breaks into several small
nuclei.

lynceus,

Fig. 55. Macronuclear reorganization prior to division in Aspidisca X1400 (Summers), a, resting nucleus; b-i, successive stages in reorganization process; j, a daughter macronucleus shortly after division.

The extrusion of a certain portion of the macronuclear material during division has been observed in a number of species. In Uroleptus halseyi, Calkins actually noticed each of the eight macronuclei
is

"purified"

by discarding a reorganization band and an "x-body"

into the cytoplasm before fusing into a single macronucleus which

then divides into two nuclei. In the more or less rounded macronucleus that is commonly found in many ciliates, no reorganization

band has been recognized.

A number of observers have however noted

150

PROTOZOOLOGY

that during the nuclear division there appears and persists a small body within the nuclear figure, located at the division plane as in
the case of Loxocephalus (Behrend), Eupoterion
blattae

Connell) and even in the widely different protozoan,

of the

(MacLennan and Endamoeba

(Kudo, 1926). Kidder (1933) observed that during the division macronucleus of Conchophthirus my till (Fig. 56), the nucleus "casts out a part of its chromatin at every vegetative division," which "is broken down and disappears in the cytoplasm of either

Fig. 56. Macronuclear division in Conchophthirus mytili,

X440 (Kidder).

daughter organism."
turbo,

similar

further in C. anodontae, C. curtus, C.

phenomenon has since been found magna (Kidder), Urocentrum

Colpidium colpoda, C. campylum, Glaucoma scintillans (Kidder Allosphaerium convexa (Kidder and Summers), Colpoda inHata, C. maupasi, Tillina canalifera, Bresslaua vorax, etc. (Burt et al., 1941). Beers (1946) noted chromatin extrusion from the macronucleus during division and in permanent cysts in Tillina magna. What is the significance of this phenomenon? Kidder and his associates believe that the process is probably elimination of waste substances of the prolonged cell-division, since chromatin extrusion does not take place during a few divisions subsequent to reorganization

and

Diller),

REPRODUCTION
after conjugation in Conchophthirus mytili

151

and since in Colpidium and Glaucoma, the chromatin elimination appears to be followed by a high division rate and infrequency of conjugation. Dass (1950) noticed a dark body between two daughter macronuclei of a ciliate designated by him as Glaucoma piriformis and considered it as surplus desoxyribonucleic acid about to be converted by the cytoplasm
to ribonucleic acid necessary for active growth.

In Paramecium aurelia, Woodruff and Erdmann (1914) reported the occurrence of "endomixis." At regular intervals of about 30 days, the old macronucleus breaks down and disappears, while each of the

two micronuclei divides twice, forming eight

disintegrate.

nuclei.

Of these,

six

The animal then

divides into two, each daughter indi-

vidual receiving one micronucleus. This nucleus soon divides twice into four, two of which develop into two macronuclei, while the

two

other two divide once more. Here the organism divides again into individuals, each bearing one macronucleus and two micronuclei.

This process, they maintained, is "a complete periodic nuclear reorganization without cell fusion in a pedigreed race of Paramecium." The so-called endomixis has since been reported to occur in many

However, as pointed out by Wilson (1928), Diller (1936), Sonneborn (1947) and others, there are several difficulties in holding
ciliates.

that endomixis

is a valid process. Diller considers that endomixis based upon partial observations on hemixis (p. 206) and autogamy (p. 203). Sonneborn could not find any indication that this process occurs in numerous stocks and varieties of Para-

may have been

mecium
cies of

aurelia, including the progeny of the strains studied by Woodruff, and maintained that endomixis does not occur in this spe-

Paramecium. As has been stated already, two types of nuclei: macronucleus and micronucleus, occur in Euciliata and Suctoria. The macronucleus
is

the center of the whole metabolic activity of the organism

absence of this nucleus, the animal perishes. The waste substances which become accumulated in the macronucleus through its manifold activities, are apparently eliminated at the time of

and

in the

division, as has

been cited above in many species. On the other under certain circumstances, the macronucleus becomes impregnated with waste materials which cannot be eliminated through this process. Prior to and during conjugation (p. 188) and autogamy (p. 203), the macronucleus becomes transhand,
it is

also probable that

formed, in
(Fig. 85)

many species,

into irregularly coiled thread-like structure

which undergoes segmentation into pieces and finally is absorbed by the cytoplasm. New macronuclei are produced from

152

PROTOZOOLOGY
of the division-products of micronuclei

some

by probably

incor-

porating the old macronuclear material. In most cases this supposition

is

not demonstrable. However, Kidder (1938) has shown

in

S'd
d
e
f
regeneration in

g
Parame-

Fig. 57. Diagram showing the macronuclear cium aurelia (Sonneborn). a, an individual before the first division after conjugation or autogamy, containing two macronuclear (stippled) anlagen, two micronuclei (rings) and about 30 disintegrating (solid black) masses of the old macronucleus; b, two individuals formed by the first division, each containing one macronuclear anlage, two micronuclei and macronuclear masses; c, two individuals produced by the second division: one (above) with the new macronucleus, two micronuclei and macronuclear masses, and the other without new macronucleus; d-f, binary fissions in which the two micronuclei divide, but old macronuclear masses are distributed equally between the two daughters until there is one large regenerated macronucleus and two micronuclei; g, division following f, goes on in an ordinary manner.

the encysted Paraclevelandia simplex, an endocommensal of the

colon of certain wood-feeding roaches, this

is

actually the case;

namely, one of the divided micronuclei fuses directly with a part of macronucleus to form a macronuclear anlage which then develops into a macronucleus after passing through "ball-of-yarn" stage similar to that which appears in an exconjugant of Nyctotherus (Fig. 85).

REPRODUCTION
tain all structures

153

then not divide mitotically as does the micronucleus? During conjugation or autogamy in a ciliate, the macronucleus degenerates, disintegrates and finally becomes absorbed in the cytoplasm. In
does
it

Since the macro-nucleus originates in a micronucleus, it which characterize the micronucleus.

must con-

Why

(Fig. 57) obexposed to 38C. from the time of the synkaryon-formation until before the second postzygotic nuclear division (a-c), the development of the two newly formed macronuclei is retarded and do not divide as usual with the result that one of the individuals formed by the second postzygotic division receives the newly formed macronucleus, while the other lacks this (c). In the latter, however, division continues, during which some of the original 20-40 pieces of the old macronucleus that have been present in the cytoplasm segregate in approximately equal number at each division (d, e) until there is only one in the animal (/). Thereafter the macronucleus divides at each division (g). Sonne-

Paramecium

aurelia,

Sonneborn (1940, 1942, 1947)

in

served that

when the animal

conjugation

is

born found this "macronuclear regeneration" in the varieties 1 and 4, but considered that it occurs in all stocks. Thus the macronucleus in this ciliate appears to be a compound structure with its 20-40 component parts, each containing all that is needed for development into a complete macronucleus. From these observations, Sonneborn concludes that the macronucleus in P. aurelia appears to undergo amitosis, since it is a compound nucleus composed of many "subnuclei" and since at fission all that is necessary to bring about genetically equivalent functional macronuclei is to segregate these
multiple subnuclei into two
division,

random groups.

While the macronuclear division usually follows the micronuclear

it takes place in the absence of the latter as seen in amicronucleate individuals of ciliates which possess normally a micronucleus. Amicronucleate ciliates have been found to occur naturally or

produced experimentally in the following species: Didinium nasutum (Thon, 1905; Patten, 1921), Oxytricha hymenostoma (Dawson, 1919), O.fallax, Urostyla grandis (Woodruff 1921), Paramecium caudatum (Landis, 1920; Woodruff, 1921), etc. Amicronucleate Oxytricha falia x which were kept under observation by Reynolds (1932) for 29 months, showed the same course of regeneration as the normal indi,

viduals. Beers (1946b) saw no difference in vegetative activity between amicronucleate and normal individuals of Tillina magna. In Euplotes patella, amicronucleates arise from "double" form (p. 229) with a single micronucleus, and Kimball (1941a) found that the

mioronucleus

is

not essential for continued

life

in at least

some

154
clones,

PROTOZOOLOGY
though
its

absence results in a marked decrease in vigor. The

bi-micronucleate Paramecium bursaria which Woodruff (1931) isolated, developed in the course of 7 years of cultivation, unimicronucleate

and

finally

amicronucleate forms, in which no marked varia-

tion in the vitality of the race

was observed. These data indicate that

if

amicronucleates are capable of carrying on vegetative activity and

multiplication, but are unable to conjugate or
cell-pairing occurs,

the result

is

abortive, though

Chen

(1940c) reported conjugation be-

tween normal and amicronucleate individuals of P. bursaria (p. 189). Horvath (1950) succeeded in destroying the micronucleus in Kahlia simplex (p. 133) and found the emicronucleates as vigorous as the normal forms, judged by the division rate, but were killed within 15 days by proactinomycin, while normal individuals resisted by encystment. This worker reasons that the emicronucleates are easily destroyed by unfavorable conditions and, therefore, ciliates without
a micronucleus occur rarely in nature.

Fig. 58. Amitosis of the vegetative nucleus in the trophozoite of

Myxosoma
Other examples

catostomi,

X2250 (Kudo).
in the vegetative nuclei in

of amitosis are

found

the trophozoite of Myxosporidia, as for example,

Myxosoma

catos-

tomi (Fig. 58), Thelohanellus notatus (Debaisieux), etc., in which the endosome divides first, followed by the nuclear constriction. In
Streblomastix strix, the

compact elongated nucleus was found to

undergo a simple division by Kof oid and Swezy.

Indirect nuclear division. The indirect division which occurs in the protozoan nuclei is of manifold types as compared with the mitosis in the metazoan cell, in which, aside from minor variations, the change is of a uniform pattern. Chatton, Alexeieff and others, have proposed several terms to designate the various types of indirect nuclear division, but no one of these types is sharply defined. For our

purpose, mentioning of a few examples will suffice. A veritable mitosis was noted by Dobell in the heliozoan Oxnerella

maritima (Fig. 59), which possesses an eccentrically situated nucleus containing a large endosome and a central centriole, from which
radiate

many axopodia

(a).

The

first

sign of the nuclear division

is

REPRODUCTION
nucleus

155

the slight enlargement, and migration toward the centriole, of the

(6). The centriole first divides into two (c, d) and the nucleus becomes located between the two centrioles (e). Presently spindle fibers are formed and the nuclear membrane disappears (/, g). After

\\m\

ymmmn
'

fin
/

Hi'

'.'.

f'n

Fig. 59. Nuclear and cytoplasmic division in Oxnerella maritime/,, X about a, a living individual; b, stained specimen; c-g, prophase; h, metaphase; i, anaphase; j, k, telophase; 1, division completed.

1000 (Dobell).

passing through an equatorial-plate stage, the two groups of 24

chromosomes move toward the opposite poles (g-i). As the spindle fibers become indistinct, radiation around the centrioles becomes conspicuous and the two daughter nuclei are completely reconstructed to assume the resting phase (j-l). The mitosis of another heliozoan Acanthocystis aculeata is, according to Schaudinn and

156

PROTOZOOLOGY
many
others, such as

from these two species, the Hartmannella (Arndt), Euglypha, Monocystis (Bglaf), Aggregata (Dobell; Bglaf;
centriole has been reported in

Stern, very similar to the above. Aside

Mitosis in Trichonympha campanula, X800 (Kofoid and resting nucleus; b-g, prophase; h, metaphase; i, j, anaphase; k, telophase; 1, a daughter nucleus being reconstructed.
Fig.
60.
a,

Swezy).

REPRODUCTION
Naville), various

157

Hypermastigina (Kofoid; Duboscq and Grasse;

Kirby; Cleveland and his associates). In numerous species the division of the centriole (or blepharoplast) and a connecting strand between them, which has been called desmose (centrodesmose or paradesmose), have been observed. According to Kofoid and Swezy (1919), in Trichonympha campanula (Fig. 60), the prophase begins early, during which 52 chromosomes
are formed and become split. The nucleus moves nearer the anterior end where the centriole divides into two, between which develops a desmose. From the posterior end of each centriole, astral rays extend out and the split chromosomes form loops and pass through "tangled skein" stage. In the metaphase, the equatorial plate is made up of V-shaped chromosomes as each of the split chromosomes is still connected at one end, which finally becomes separate in anaphase, followed by reformation of two daughter nuclei. As to the origin and development of the achromatic figure, various observations and interpretations have been advanced. Certain Hypermastigina possess very large filiform centrioles and a large rounded nucleus. In Barbulanympha (Fig. 61), Cleveland (1938a) found that the centrioles vary from 15 to 30^ in length in the four species of the genus which he studied. They can be seen, according to Cleveland, in
life

as

made up

of

a dense hyaline protoplasm.

becomes apparent that the two centrioles are joined at their anterior ends by a desmose and their distal ends 20 to 30/x apart, each of which is surrounded by a special centrosome (a). In the resting stage no fibers extend from either centriole, but in the prophase, astral rays begin to grow out from the distal end of each centriole (6). As the rays grow longer (c), the two sets soon meet and the individual rays or fibers join, grow along one another and overlap to form the central spindle (d). In the resting nucleus, there are large irregular chromatin granules which are connected by fibrils with one another and also with the nuclear membrane. As the achromatic figure is formed and approaches the nucleus, the chromatin becomes arranged in a single spireme imbedded in matrix. The spireme soon divides longitudinally and the double spireme presently breaks up transversely into paired chromosomes. The central spindle begins to compress the nuclear membrane and the chromosomes become shorter and move apart. The intra- and extra-nuclear fibrils unite as the process goes on (e), the central spindle now assumes an axial position, and two groups of V-shaped chromosomes are drawn to opposite poles. In the telophase, the chromosomes elongate and become branched, thus assuming conditions seen in the resting nucleus.
stained,
it

When

158

PROTOZOOLOGY

Fig. 61. Development of spindle and astral rays during the mitosis in Barbulanympha, X930 (Cleveland), a, interphase centrioles and centrosomes; b, prophase centrioles with astral rays developing from their distal ends through the centrosomes; c, meeting of astral rays from two centrioles; d, astral rays developing into the early central spindle; stage showing the entire mitotic figure.
e,

a later

In Holomastigotoides tusitala (Fig. 172, a, b), Cleveland (1949) brought to light the formation of the achromatic figure, and the minute structure and change in chromosomes (Fig. 62). In the late telophase, after cytoplasmic division, the centrioles follow the flagellar

bands 4 and 5 for 1.5 turns (a). The two chromosomes are anchored to the old centriole. When the new centriole has become as

REPRODUCTION

159

M>,

Fig. 62. Mitosis in Holomastigotoides tusitala (Cleveland), a, anterior region showing flagellar bands, centrioles, centromeres and chromosomes, b-h, telophase; i, j, prophase; k, metaphase; 1, anaphase; m, telophase, b, c, new and old centrioles forming achromatic figure; d, one chromosome has shifted its connection from old to new centriole; e, f, flattening out of
centrioles
ing;
i,

and achromatic figure; g, h, beginning of chromosomal twistchromosomes duplicated, producing many gyres of close-together relational coiling of chromatics, and centromeres duplicated; j, chromatids losing their relational coiling by unwinding; k, relational coiling disappeared, achromatic figure elongating and separating sister chromatids; central spindle bent, chromatids in two groups; m, central spindle 1,
pulled apart.

160

PROTOZOOLOGY

long as the old one, the centrioles begin to produce astral rays (b) which soon meet and form the central spindle (c). An astral ray from
the new centriole becomes connected with the centromere of one of the chromosomes (d). The spindle grows in length and enters resting stage (e-j), later the spindle fibers lengthen (k, /) and pull apart (m). The chromosome is composed of the matrix and chromonema

which the former disintegrates in the telophase and reappears in the early prophase of each chromosome generation, while the latter remains throughout. From late prophase to mid-telophase, minor coils are incorporated in major coils (a-c) from mid-telophase to late telophase, they are in very loose majors (d); and after the majors have disappeared completely, they become free (e). Soon
(Fig. 63), of
;

after cytoplasmic division, the majors

become

looser

and

irregular

minors and twisting remain. Each chromosome presently divides into 2 chromatids (f) and a new matrix is formed for each. As the matrix contracts the chromatids lose their relational coiling and the minors become bent and thus the new generation of major coils makes its appearance (g). With the further concentration of the matrix, the majors become more conspicuous

and

finally disappear, while

(h),

lational coiling has

the minors being incorporated into them. When most of the rebeen lost and majors are close together, the
for

chromosomal changes cease

days or weeks. This

is

the late pro-

phase. After the resting stage, the achromatic figure commences to grow again (i, j) and the two groups of chromatids are carried to the
poles, followed
coils

by transverse cytoplasmic

division (Fig. 64).

The

remain nearly the same during metaphase to early telophase. Thus Cleveland showed the continuity of chromosomes from generation to generation.

He

finds that the resting stage of

chromosomes
rest in inter-

varies in different types of cells:

some chromosomes

prophase and others in telophase, and that the centromere is an important structure associated with the movement of chromatids and in the reduction of chromosomes in meiosis. For
phase,

some

in early

fuller

information the reader

is

referred to the profusely illustrated

initiated

original paper (Cleveland, 1949).

In Lophomonas by the migration

blattarum, the nuclear division (Fig. 65)

of the nucleus out of the calyx.

is

On

the nuclear

membrane is attached the centriole which probably originates in the blepharoplast ring; the centriole divides and the desmose which grows, now stains very deeply, the centrioles becoming more conspicuous in the anaphase when new flagella develop from them.
Chromatin granules become larger and form a spireme, from which

REPRODUCTION

161

?,

aft

Fig. 63. Chromosomal changes in Holomastigotoides tusitala, X1050 (Cleveland), a, telophase shortly after cytoplasmic division, new fifth band and new centriole are growing out and chromosomes are twisted; b, c, the same chromosome showing major and minor coils respectively; d, later telophase, showing minor coils; e, matrix completely disintegrated, showing minor coils; f, a prophase nucleus, showing division of chromosomes into two chromatids; g, later prophase, in which majors are developing with minors; h, later prophase; i, metaphase in which distal halves of the chromatids have not yet separated, showing minor
coils;
j,

anaphase, showing major and minor

coils of

chromonemata.

162

PROTOZOOLOGY

Fig. 64. Cytoplasmic division in Holomastigotoides tusitala, X about 430 (Cleveland), a, fifth flagellar band has separated from others; b, one nucleus and fifth band moving toward posterior end; c, the movement of the band and nucleus has been completed; d, e, anterior and posterior daughter individuals, produced by transverse division.

REPRODUCTION

163

6-8 chromosomes are produced. Two groups of chromosomes move toward the opposite poles, and when the division is completed, each centriole becomes the center of formation of all motor organellae. In some forms, such as Noctiluca (Calkins), Actinophrys (Belaf), etc., there may appear at each pole, a structureless mass of cytoplasm (centrosphere), but in a very large number of species there

a,

Fig. 65. Nuclear division in Lophomonas blattarum, X1530 (Kudo), resting nucleus; b, c, prophase; d, metaphase; e-h, anaphase; i-k, telophase.

appear no special structures at poles and the spindle fibers become stretched seemingly between the two extremities of the elongating nuclear membrane. Such is the condition found in Pelomyxa (Kudo) (Fig. 66), Cryptomonas (Belaf), Rhizochrysis (Doflein), Aulacantha (Borgert), and in micronuclear division of the majority of Euciliata and Suctoria. The behavior of the endosome during the mitosis differs among different species as are probably their functions. In Eimeria schubergi (Schaudinn), Euglena viridis (Tschenzoff), Oxyrrhis marina (Hall),

164

PROTOZOOLOGY

Colacium vesiculosum (Johnson), Haplosporidium limnodrili (Gran-

endosome divides by elongation and constriction along with other chromatic elements, but in many other cases, it disappears during the early part of division and reapata), etc., the conspicuously staining

pears

when the daughter nuclei are reconstructed as observed in Monocystis, Dimorpha, Euglypha, Pamphagus (Belar), Acanthocystis (Stern),

Chilomonas (Doflein), Dinenympha (Kirby),

etc.

Fig. 66. Mitosis in Pelomyxa carolinensis, X1150 (Kudo), a, c, 1, in life; d-k, in acidified methyl green, a, b, resting nuclei; c-g, prophase; h, metaphase; i-k, anaphase; 1, front and side view of a young daughter
b,

nucleus.

In the vegetative division of the micronucleus of Conchophthirus

anodontae, Kidder (1934) found that prior to division the micronucleus moves out of the pocket in the macronucleus and the chromatin

becomes irregularly disposed in a reticulum; swelling continues and the chromatin condenses into a twisted band, a spireme, which breaks into many small segments, each composed of large chromatin granules. With the rapid development of the spindle fibers, the twelve bands become arranged in the equatorial plane and condense. Each chromosome now splits longitudinally and two groups of 12 daughter chromosomes move to opposite poles and transform them-

REPRODUCTION
selves into

105 detailed study of micro-

two compact daughter

nuclei.

nuclear division (Fig. 67) of Urostyla grandis was made by Raabe (1946). The micronucleus is a compact body in the interphase (a),

a, resting

Fig. 67. Micronuclear division of Urostyla grandis, X2100 (H. Raabe). stage; b-j, prophase (b-e, stages in the formation of spireme; f, g, spireme ribbon; h, i, twelve segments of ribbon arranged in the direction of the elongating nuclear axis; j, a polar view of the same); k, 1,

metaphase, condensation of the segments; m-o, anaphase; p, late anaphase; q, a daughter nucleus in telophase; r-t, reconstruction stages; u, a resting daughter nucleus.

166

PROTOZOOLOGY

but increases in size and the chromatin becomes grouped into small masses (6, c), which become associated into a spiral ribbon (d-g). The latter then breaks up into 12 segments that are arranged parallel to the axis of the elongating nucleus (h-i). Each segment condenses into a chromosome which splits longitudinally into two (k) and the two groups of chromosomes move to opposite poles (l-P). In Zelleriella elliptica (Fig. 295) and four other species of the genus inhabiting the colon of Bufo valliceps, Chen (1936, 1948) observed the formation of 24 chromosomes, each of which is connected with a fiber of the intranuclear spindle and splits lengthwise in the metaphase.

While
vision.

in the

majority of protozoan mitosis, the chromosomes

split

longitudinally, there are observations which suggest a transverse di-

As examples may be mentioned the chromosomal

divisions in

number number of species observations vary within a species, as, for example, in Peranema trichophorum in which the chromosomes were observed to divide transversely (Hartmann and
Astasia laevis (Belaf), Entosiphon sulcatum (Lackey), and a
of ciliates. In a small

Chagas) as well as longitudinally (Hall and Powell; Brown). It

of

is

inconceivable that the division of the chromosome in a single species

organism

is

haphazard. The apparent transverse division might be

explained by assuming, as Hall (1937) showed in Euglena gracilis, that the splitting is not completed at once and the pulling force acting upon them soon after division, brings forth the long chromo-

somes

still

connected at one end. Thus the chromosomes remain to-

gether before the anaphase begins. In the instances considered on the preceding pages, the so-called

chromosomes found

in

them, appear to be essentially similar

in

structure and behavior to typical metazoan chromosomes. In

many

other cases, the so-called chromosomes or "pseudochromosomes" are slightly enlarged chromatin granules which differ from the ordin-

ary chromatin granules in their time of appearance and movement only. In these cases it is of course not possible at present to determine how and when their division occurs before separating to the respective division pole. In Table 5 are listed the number of the
in

"chromosomes" which have been reported by various investigators the Protozoa that are mentioned in the present work.
Cytoplasmic division

The

division of the nucleus

is

accompanied by division
of the ciliates

of extranu-

clear organelles such as chromatophores, pyrenoids, etc.

The blephaundergo
di-

roplast of the flagellates

and kinetosomes


REPRODUCTION
Table
Protozoa
5.

167

Chromosomes in Protozoa

168


REPRODUCTION
Table
Protozoa
5.

Continued
of

Number

chromosomes

Observers

Chilodonella uncinata

170

PROTOZOOLOGY
body in Cochliopodium, homogeneous test also divides
is

as in Arcella, Pyxidicula, Euglypha, etc. According to Doflein, the

division plane coincides with the axis of

Pseudodifflugia, etc.,
into

and the

delicate

two

parts. In the majority of the Mastigophora, the division

is

longitudinal, as

shown by that
is

of

Rhabdomonas incurva

(Fig. 69).
etc.,

In certain dinoflagellates, such as Ceratium, Cochliodinium,

the division plane
oblique, while in forms such as Oxyrrhis

(Dunk-

b ^

ssfisSk

Fig. 68. External morphological changes during division of

proteus, as

Amoeba

viewed in

life

in reflected light,

about 20 (Chalkley and

Daniel),
stage;
c,

a,

prior to elongation; d, further elongation;

shortly before the formation of the division sphere; b, a later e, division almost

completed.

erly; Hall), the fission is transverse. In Streblomastix strix (Kofoid

and Swezy, 1919), Lophomonas

striata

(Kudo, 1926b), Spirotrichoclavellinae

nympha
64)

bispira (Cleveland, 1938),

Holomastigotoides tusitala (Fig.

and others (Cleveland,

1947),

and Strombidium

(Bud-

denbrock, 1922), the division takes place transversely but the polarity of the posterior individual is reversed so that the posterior end of the parent organism becomes the anterior end of the posterior daughter individual. In the ciliate Bursaria, Lund (1917), observed
reversal of polarity in one of the daughter organisms at the time of
division of

after being cut into one-half the

normal individuals and also in those which regenerated normal size.

REPRODUCTION
In the Ciliophora the division
is

171

as a rule transverse (Fig. 52), in

which the body without any enlargement or elongation divides by constriction through the middle so that the two daughter individuals are about half as large at the end of division. Both individuals
usually retain their polarity.

Multiple division. In multiple division the body divides into a

number

of

daughter individuals, with or without residual cyto-

Fig. 69. Nuclear

X
e,

and cytoplasmic division in Rhabdomonas incurva, about 1400 (Hall), a, resting stage; b, c, prophase; d, equatorial plate; f, anaphase; g, telophase.

plasmic masses of the parent body. In this process the nucleus may undergo either simultaneous multiple division, as in Aggregata,
or

more commonly, repeated binary

fission, as in

Plasmodium

(Fig.

256) to produce large numbers of nuclei, each of which becomes the center of a new individual. The number of daughter individuals often
varies, not only

among

the different species, but also within one and

the same species. Multiple division occurs

commonly

in the

Fora-

minifera (Fig. 208); the Radiolaria (Fig. 218), and various groups of Sporozoa in which the trophozoite multiplies abundantly by this

method. Budding. Multiplication by budding which occurs in the Protozoa is the formation of one or more smaller individuals from the

172

PROTOZOOLOGY
is

parent organism. It

either exogenous or endogenous, depending

upon the location

buds or gemmules. Exogenous budding has been reported in Acanthocystis, Noctiluca (Fig. 127), Myxosporidia (Fig. 70, b), astomatous ciliates (Fig. 298), Chonotricha, Suctoria (Fig. 371, k), etc. Endogenous budding has been
of the developing

lit

/im
Fig. 70. a, b, budding in

Chloromyxum

leydigi;

e,

Myxidium lieberkiihni; c, d, plasmotomy plasmotomy in Sphaeromyxa balbianii.

in

in Testacea, Gregarinida, Myxosporidia (Figs. 279, e; 281, j), and other Sporozoa as well as Suctoria (Fig. 371, h). Collin observed a unique budding in Tokophrya cyclopum in which the entire body, excepting the stalk and pellicle, transforms itself into a young ciliated bud and leaves sooner or later the parent pellicle. Plasmotomy. Occasionally the multinucleate body of a protozoan divides into two or more small, mutinucleate individuals, the cyto-

found

plasmic division taking place independently of nuclear division. This has been called plasmotomy by Doflein. It has been observed in the

REPRODUCTION

173

trophozoites of several coelozoic myxosporidians, such as Chloromyxumleydigi, Sphaeromyxa balbianii (Fig. 70), etc. It occurs further
in certain Sarcodina such as
(Fig. 71),

Mycetozoa

(Fig. 179)

and Pelomyxa

and

Protociliata.

in culture dishes, in

Fig. 71. Eight individuals of Pelomyxa carolinensis, seen undisturbed which mitotic stages occurred as follows, X40 (Kudo) a, early prophase; b, c, later prophase; d, metaphase; e, f, early and late anaphase; g, h, late telophase to resting nuclei (g, plasmotomy into two
individuals; h,

plasmotomy

into three daughters).

Colony formation

When

the division

is

the daughter individuals, a colonial form

repeated without a complete separation of is produced. The compon-

174

PROTOZOOLOGY
may either have protoplasmic connections
if

ent individuals of a colony

among them

or be grouped within a gelatinous envelope

completely

separated. Or, in the case of loricate or stalked forms, these exoskeletal structures

may become

attached to one another. Although

varied in appearance, the arrangement and relationship of the com-

ponent individuals are constant, and this makes the basis for distinguishing the types of protozoan colonies, as follows: Catenoid or linear colony. The daughter individuals are attached endwise, forming a chain of several individuals. It is of comparatively uncommon occurrence. Examples: Astomatous ciliates such as Radiophrya (Fig. 298), Protoradiophrya (Fig. 298) and dinoflagellates such as Ceratium, Haplozoon (Fig. 130) and Polykrikos (Fig.
132).

Arboroid or dendritic colony. The individuals remain connected with one another in a tree-form. The attachment may be by means of the lorica, stalk, or gelatinous secretions. It is a very common
colony found in different groups. Examples: Dinobryon (Fig. 108), Hyalobryon (Fig. 108), etc. (connection by lorica); Colacium (Fig.
121),

many

Peritricha (Figs. 362; 364), etc. (by stalk); Poterioden-

Stylobryon (Fig. 151), etc. (by lorica and stalk); Hydrurus (Fig. 109), Spongomonas (Fig. 150), Cladomonas(Fig. 150) and Anthophysis (Fig. 151) (by gelatinous secretions).

dron

(Fig. 139),

Discoid colony.
single plane

small

number

of individuals are

arranged in a

and grouped together by a gelatinous substance. Exam-

ples: Cyclonexis (Fig. 108),

Gonium

(Fig.

116), Platydorina (Fig.

117), Protospongia (Fig. 138), Bicosoeca (Fig. 139), etc.

Spheroid colony. The individuals are grouped in a spherical form. Usually enveloped by a distinct gelatinous mass, the component individuals may possess protoplasmic connections among them. Examples: Uroglena (Fig. 108, c), Uroglenopsis (Fig. 108, d), Volvox
(Fig. 115), Pandorina (Fig. 117,/), Eudorina (Fig. 117, h), etc. Such forms as Stephanoon (Fig. 117, a) appear to be intermediate between this and the discoid type. The component cells of some spheroid colonies show a distinct differentiation into somatic and reproductive individuals, the latter developing from certain somatic cells during

the course of development.

is sometimes spoken of, is a loose one species, usually of Sarcodina, which become attached to one another by means of pseudopodia in an ir-

The gregaloid

colony, which

group

of individuals of

regular form.

REPRODUCTION
Asexual reproduction

175

The Protozoa nourish themselves by certain methods, grow and multiply, by the methods described in the preceding pages. This
phase of the
trophozoite.
life-cycle of

a protozoan

is

the vegetative stage or the

The trophozoite repeats

its

asexual reproduction process

under favorable circumstances. Generally speaking, the Sporozoa

ncrease to a

much greater number by multiple division or schizogony and the trophozoites are called schizonts. Under certain conditions, the trophozoite undergoes encystment (Fig. 72). Prior to encystment, the trophozoites cease to ingest, and extrude remains of, food particles, resulting in somewhat smaller forms which are usually rounded and less active. This phase is some-

Fig. 72. Encystment of

Lophomonas

blattarum,

X1150 (Kudo).
de-

times called the precystic stage.

differentiated;

The whole organism becomes

cell

namely, various
peristome,
etc.,

organs such as

cilia,

cirri,

flagella, axostyle,

become usually absorbed. Finally

the organism secretes substances which become solidified into a resistant wall, and thus the cyst is formed. In this condition, the

protozoan is apparently able to maintain its vitality for a certain length of time under unfavorable conditions. Protozoa appear to encyst under various conditions. Low temperature (Schmahl, 1926), evaporation (Belaf, 1921; Bodine, 1923; Garnjobst, 1928), change in pH (Koffman, 1924; Darby, 1929), low or high oxygen content (Brand, 1923; Rosenberg, 1938), accumulation of metabolic products (Belaf, 1921;

Mast and

Ibara, 1923;

Beers, 1926) or of associated bacteria (Mouton, 1902; Belaf, 1921)

and over-population (Barker and Taylor, 1931) in the water in which Protozoa live, have been reported to bring about encystment. While

17(3

PROTOZOOLOGY
by many observers
Kidder, 1941; Singh, 1941; Beers, as a cause of encystment in a number of Protozoa such

lack of food in the culture has been noted

(Oehler, 1916; Claff,

Dewey and

1948; etc.)

and Burroughs, Didinium (Mast and Ibara, 1931), Uroleptus (Calkins, 1933), etc., an abundance of food and adequate nourishment seem to be prerequisite for encystment. Particular food was found in some instances to induce encystment. For example, Singh (1948) employed for culture of Leptomyxa reticulata, 40 strains of bacteria, of which
as Blepharisma (Stolte, 1922), Polytomella (Kater
1926),

15 led to the production of a large

number

of cysts in this sarcodinan.

Encystment

of

Entamoeba

histolytica is easily

obtained by adding

starch to the culture (Dobell and Laidlow, 1926; Balamuth, 1951).

if kept under favorable conditions, does not Didinium after 750 generations, according to Beers (1927), showed practically the same encystment rate as those which had passed through 10 or 20 generations since the last encystment. When Leptomyxa mentioned above is cultured for more than a year, no encystment occurred, but young cultures when supplied

The age

of culture,

influence encystment.

with certain bacteria encysted (Singh, 1948). In some cases, the organisms encyst temporarily in order to un-

dergo nuclear reorganization and multiplication as in Colpoda (Fig. 73) (Kidder and Claff, 1938; Stuart, Kidder and Griffin, 1939), Tillina (Beers, 1946), etc. In Ichthyophthirius, the organism encysts after leaving the host fish and upon coming in contact with a solid
object,

1937).
its

and multiplies into numerous "ciliospores" (MacLennan, Pelomyxa carolinensis (Illinois stock) has not encysted since

discovery in 1944, although the cultures were subjected to vari-

ous environmental changes, but P. illinoisensis has been found to

encyst and excyst frequently in flourishing cultures (Kudo, 1951).

Thus

it

may

be assumed that some unknown internal factors play

as great a part as do the external factors in the

phenomenon

of en-

cystment (Ivanic, 1934; Cutler and Crump, 1935). The cyst is covered by one to three membranes. Though generally homogeneous, the wall of cyst may contain siliceous scales as in Euglypha (Fig. 74). While chitinous substance is the common material of which the cyst wall is composed, cellulose makes up the cyst membrane of many Phytomastigina. Entz (1925) found the cysts of various species of Ceratium less variable in size as compared with the vegetative form, and found in all, glycogen, oil and
volutin.

The capacity

of

Protozoa to produce cyst

is

probably one of the

REPRODUCTION
reasons
globe.

177

why they

are so widely distributed over the surface of the

The minute protozoan cysts are easily carried from place to place by wind, attached to soil particles, debris, etc., by the flowing water of rivers or the current in oceans or by insects, birds, other

life cycle of Colpoda cucullus (Kidder and normal reproductive activity repeated (j-b) under favorable cultural conditions; k-o, resistant cyst (k-n, nuclear reorganization and chromatin elimination).

Fig. 73.

Diagram showing the

Claff). a-j,

animals to which they become readily attached. The cyst is capable of remaining viable for a long period of time eight years in Haema:

tococcus pluvialis (Reichenow, 1929), four yaers in

Spathidium spath-

ula and Oxytricha sp.

Colpoda cucullus

(Dawson and Mitchell, 1929), five years in (Dawson and Hewitt, 1931), 10 years in Didinium
etc.

nasutum (Beers, 1937),

178

PROTOZOOLOGY

When a cyst encounters a proper environment, redifferentiation takes place within the cyst. Various organellae which characterize
the organism, are regenerated and reformed, and the young trophoreturns once more to its trophic Experimental data indicate that excystment takes place under conditions such as addition of fresh culture medium (Kiihn, 1915; Rosenberg, 1938), hypertonic solution (Ilowaisky, 1926), distilled water (Johnson and Evans, 1941), organic infusion (Mast, 1917; Beers, 1926; Barker and Taylor, 1933), and baczoite excysts.

The emerged organism

phase

of existence.

terial infusion (Singh, 1941; Beers,

1946a) to the culture medium.

Change in pH (Koffman, son and Evans, 1941) and

Finley, 1936) of the

1924), lowering the temperature (John-

increase in oxygen content (Brand, 1923;

also been reported as bringing Colpoda cucullus is said to be due

medium have
in

about excystment. Excystment

Fig. 74.

Encystment

of

Euglypha acanthophora, X320 (Kiihn).

to specific inducing substances present in plant infusion

(Thimann and Barker, 1934; Haagen-Smit and Thimann, 1938). Experimenting with two soil amoebae, "species 4 and Z," Crump (1950) found that the excystment in species Z took place without the presence of bacteria and regardless of the age of the cysts, but species 4 excysted
only in the presence of certain bacteria (Aerobacter sp. or "4036")

and the excystment diminished with the age of cysts. Crump suggested that the two strains of bacteria appeared to produce some material which induced excystment in Amoeba species 4. In Tillina magna, Beers (1945) found, however, the primary excystment-inducing factor to be of an osmotic nature and inducing substances,
a secondary one.
aperture or apertures are formed in the cyst wall emergence of the content, precise information is not yet on hand, though there are many observations. In the excystment in Didinium and Tillina, Beers (1935, 1945, 1945a) notes that
to
prior to the

As

how an

REPRODUCTION

179

an increased internal pressure due to the imbibition of water, results in the rupture of the cyst wall which had lost its rigidity and

Pelomyxa illiby pseudopodial pressure (Kudo, 1951). Seeing a similar aperture formation in the cyst of Entamoeba histolytica, Dobell (1928) "imagined that the amoeba secretes a ferment which dissolves the cyst wall."
resistance (Fig. 75). Apertures in the cyst wall of
noisensis are apparently produced

Fig. 75.
vidual,

Excystment

in

Didinium nasutum, as seen

in a single indi-

appearance of "excystment" vacuole; c, rupture of the cyst membrane, the vacuole is becoming enlarged; d, e, emergence of the cyst content, the vacuole increasing in size; f, the empty outer cyst membrane; g, the free organism with the inner membrane; h, organism after discharge of vacuole; i, j, later stages of emergence of the ciliate.
(Beers), a, resting cyst; b,

X250

Although encystment seems to be an essential phase

such

in the life

cycle of Protozoa in general, there are certain Protozoa including

mecium

widely distributed forms as the species of Paraphenomenon has not been definitely observed (p. 744). In some Sporozoa, encystment is followed by production of large numbers of spores, while in others there is no encystment.
in

common and
which

this

Here at the end

of active multiplication of trophozoite, sexual re-

180

PROTOZOOLOGY

production usually initiates the production of the spores (Fig. 76). The spores which are protected by a resistant membrane are capable of remaining viable for a long period of time outside the host

body.

a,

Fig. 76. Diagram illustrating the life-cycle of Thelohania legeri (Kudo), extrusion of the polar filament in gut of anopheline larva; b, emerged
c-f,

amoebula;

schizogony in fat body; g-m, sporont-formation; m-x,

stages in spore-formation.

Sexual reproduction and life-cycles

Besides reproducing by the asexual method, numerous Protozoa

reproduce themselves in a manner comparable with the sexual reproduction which occurs universally in the Metazoa. Various types
of sexual reproduction have been reported in literature, of which a few will be considered here. The sexual fusion or syngamy which is a complete union of two gametes, has been reported from various groups, while the conjugation which is a temporary union of two individuals for the purpose of exchanging the nuclear material, is found almost exclusively in the Ciliophora. Sexual fusion. The gametes which develop from trophozoites, may be morphologically alike (isogametes) or unlike (anisogametes)

REPRODUCTION

181

both of which are, in well-studied forms, physiologically different as judged by their behavior toward each other. If a gamete does not meet with another one, it perishes. Anisogametes are called microgametes and macrogametes. Difference between them is comparable in many instances (Figs. 77, 256) with that which exists between the spermatozoa and the ova of Metazoa. The microgametes are motile, relatively small and usually numerous, while the macrogametes are usually not motile, much more voluminous and fewer in number. Therefore, they have sometimes been referred to as male and female
gametes
(Fig. 77).

^^
Fig. 77.
a,

macrogamete, and

b,

microgamete

of Volvox aureus,

X1000

(Klein).

While morphological differences between the gametes have long been known and studied by many workers, whatever information we possess on physiological differences between them is of recent origin. Since 1933, Moewus and his co-workers have published a series of papers based upon their extended studies of bacteria-free cultures of many species (and strains) of Chlamydomonas (p. 276) which throw some light on the gamete differentiation among these phytomonadinans. The gametes in Chlamydomonas are mostly
isogamous, except in a few forms. Sexual fusion takes place in the majority of species and strains between the gametes produced in
different clones,

Moewus

and there is no gametic fusion within a single clone. obtained "sex substances" from some of the cultures and

showed that these are chemotactic substances. Each gamete secretes substances that attract the other and each reacts to the substances secreted by the other. Kiihn, Moewus and Wendt (1939) recognized "hormones," and named them, termones (sex-determining hormones), anderotermone (male-determining hormone) and gynoter-

mone (female-determining hormone).

In a few strains or species of Chlamydomonas, sexual fusion is found to take place among the gametes that develop within a single
clone.

Moewus
in

gametes

considers in these cases there exist two types of a clone. However, Pascher, Pringsheim, and others ob-

182

PROTOZOOLOGY

Fig. 78. Sexual fusion in Copromonas subtilis,

X1300
is

(Dobell).

tained results which seem to indicate that there

no physiological

or sex differentiation between the fusing gametes. In the muchstudied Sporozoa, for example, Plasmodium, the two gametes are both morphologically and physiologically differentiated, and sexual fusion always takes place between two anisogametes.

Fig. 79. Sexual fusion in Trinema linearis, X960 (Dunkerly). a, an organism in life, with the resting nucleus and two contractile vacuoles; b, union of two individuals; c, fusion of the organisms in one test, surrounded by cyst membrane; d, older cyst; e, still older cyst with a single
nucleus.

REPRODUCTION
The isogamy
monas
is

183

typically represented

subtilis (Fig. 78), in

by the flagellate Coprowhich there occurs, according to Dobell,

Fig. 80.

The life-cycle of Stephanosphaera pluvialis (Hieronymus). a-e, asexual reproduction; f-m, sexual reproduction.

a complete nuclear and cytoplasmic fusion between two isogametes. Each nucleus, after casting off a portion of its nuclear material,
fuses with the other, thus forming a zygote containing a synkaryon.

In Trinerna lineare (Fig. 79), Dunkerly (1923) saw isogamy in which

Fig. 81. Sexual reproduction in Trichonympha of Cryptocercus (Cleveland), a, vegetative individual; b, gametocyte in early stage of encystment; c, anterior end of the same organism (chromosomes have been duplicated, nuclear sleeve is opening at seams and granules are flowing into the cytoplasm); d, further separation of the male and female chromosomes; e, the nuclear division has been completed, few old flagella remain and new post rostral flagella are growing; f, the cytoplasmic division has begun at the anterior end; g, the gametes just before excystment, the female showing the developing ring of fertilization granules; h, a female gamete; i, a female gamete with a fertilization ring, a, X350;
b,

X320;

c,

X600;

d-i,

X280.

REPRODUCTION
two individuals undergo a complete fusion within one
cyst.

185
test

and en-

In Stephanosphaera pluvialis (Fig. 80), both asexual and sexual reproductions occur, according to Hieronymus. Each individual multiplies and develops into numerous biflagellate gametes, all of which are alike. Isogamy between two gametes results in formation of numerous zygotes which later develop into trophozoites. Anisogamy has been observed in certain Foraminifera. It perhaps occurs in the Radiolaria also, although positive evidence has yet to be presented. Anisogamy seems to be more widely distributed. In

Pandorina morum, Pringsheim observed that each cell develops asexyoung colony or into anisogametes which undergo sexual fusion and encyst. The organism emerges from the cyst and develops into a young trophozoite. A similar life-cycle was found by Goebel in Eudorina elegc.ns The wood-roach inhabiting flagellates belonging to Trichonympha, Oxymonas, Saccinobaculus, Notila and Eucomonympha, were found by Cleveland (1949a-1951a) to undergo sexual reproduction when the host insect molts. It has been observed that the gamete-formation is induced by the molting hormone produced by the prothoracic glands of the host insect. The sexual reproduction of Trichonympha, possessing 24 chromosomes, as observed and described by Cleveland, is briefly as follows (Figs. 81, 82): About three days before its host molts, the haploid nucleus in the flagellate divides, in which two types of daughter chromosomes (or chromatids) become separated from each other: the dark-staining male gamete nucleus and light-staining female gamete nucleus (Fig. 81, b-d); in the meantime, a membrane is formed to envelop the organism (b, d). When the cytoplasmic division is completed (e-g), the two gametes "exually into a

cyst" and become free in the host gut (h; Fig. 82,

b).

In the female

gamete, there appear "fertilization granules" (Fig. 81, h), which gather at the posterior extremity (i), through which a fluid-filled vesicle ("fertilization cone") protrudes (Fig. 82, a). A male gamete
(6)

comes

in

touch with a female gamete only at this point

(c),

and

enters the latter (d-f).

The two gamete

nuclei fuse into a diploid

synkaryon

(g, h).

increase in size,

The zygote and its nucleus begin immediately to and undergo two meiotic divisions (i-k), finally givis

ing rise to vegetative individuals (Fig. 81, a).

Among

the Sporozoa, anisogamy

of
in

common

occurrence. In
(Fig.

Coccidia, the process

was well studied

Eimeria schubergi

243), Aggregata eberthi (Fig. 246), Adelea ovata (Fig. 253), etc.,
or sporozoites develop. Similarly in

and

the resulting products are the oocysts (zygotes) in which the spores

Haemosporidia such as Plasmo-

186

PROTOZOOLOGY

Fig. 82. Sexual reproduction in Trichonympha of Cryptocercus (Cleveland), a, a female gamete with a fetilization ring and cone; b, a male gamete; c-g, stages in fusion and fertilization; h, a zygote; i, telophase of the first meiotic division of the zygote nucleus; j, k, prophase and anaphase of the second meiotic division, a-g, X280;h, X215;i-k, X600.

REPRODUCTION
dium
vivax (Fig. 256),

187

anisogamy

results in the formation of the

ookinetes or motile zygotes which give rise to a large number of sporozoites. Among Myxosporidia, a complete information as to

how
tion,

the initiation of sporogony

is still

is

associated with sexual reproduc-

lacking. Naville, however, states that in the trophozoite

Sphaeromyxa sabrazesi (Fig. 277), micro- and macro-gametes develop, each with a haploid nucleus. Anisogamy, however, is peof

culiar in that the

two nuclei remain independent. The microgametic

nucleus divides once and the two nuclei remain as the vegetative nuclei of the pansporoblast, while the macrogamete nucleus multiplies

repeatedly and develop into two spores. Anisogamy has been

suggested to occur in some

members of Amoebina, particularly in Endamoeba blattae (Mercier, 1909). Cultural studies of various parasitic amoebae in recent years show, however, no evidence of sexual
reproduction.

Among

the Ciliophora, the sexual fusion occurs only

in Protociliata (Fig. 294).

is a temporary union of two indivisame species for the purpose of exchanging part of the nuclear material and occurs almost exclusively in the Euciliata and Suctoria. The two individuals which participate in this process may be either isogamous or anisogamous. In Paramecium caudatum (Fig. 83), the process of conjugation has been studied by

Conjugation. The conjugation

duals of one and the

many

and Cull

workers, including Biitschli (1876), Maupas (1889), Calkins (1907), and others. Briefly the process is as follows: Two

similar individuals

come

in contact

on their oral surface

(a).

The

micronucleus in each conjugant divides twice (b-e), forming four micronuclei, three of which degenerate and do not take active part during further changes (f-h). The remaining micronucleus divides

once more, producing a wandering pronucleus and a stationary pronucleus (/, g). The wandering pronucleus in each of the conjugants enters the other individual and fuses with its stationary pronucleus

The two conjugants now separate from each other and become exconjugants. In each exconjugant, the synkaryon divides three times in succession (i-m) and produces eight nuclei (n), four
(h, r).

which remain as micronuclei, while the other four develop into (o). Cytoplasmic fision follows then, producing first, two individuals with four nuclei (p) and then, four small individuals, each containing a micronucleus and a macronucleus (a). Jennings maintained that of the four smaller nuclei formed in the exconjugant (o), only one remains active and the other three deof

new macronuclei

generate. This active nucleus divides prior to the cytoplasmic divi-

188

PROTOZOOLOGY

Fig. 83. Diagram illustrating the conjugation of Paramecium caudatum. a-q, X about 130 (Calkins); r, a synkaryon formation as in h, X1200

(Dehorne).

REPRODUCTION

1S9

sion so that in the next stage (p), there are two developing macronuclei and one micronucleus which divides once more before the

second and last cytoplasmic division (q). During these changes, the original macronucleus disintegrates, degenerates, and finally becomes absorbed in the cytoplasm.

Although

this

is

the general course of events in the conjugation

of this ciliate, recent observations revealed a

number

of different

nuclear behavior. For example, there

in self fertilization (Diller,

may

not be pronuclear exp. 204),

change between the conjugants (cytogamy,

1950a). In a

thus resulting
Diller
divifirst

number

of races,

(1950) found that one of the

two nuclei produced by the

sion of the synkaryon degenerates, while the other nucleus divides

three times, forming 8 nuclei, and furthermore, an exconjugant

zation has been completed.

may

conjugate occasionally with another individual before the reorgani-

The conjugaton

of

P. bursaria has also received attention of

many

workers. According to
is

division

a long process.

Chen (1946a), the first micronuclear One daughter nucleus degenerates and
wan-

the other undergoes a second division. Here again one nucleus degenerates, while the other divides once more, giving rise to a

dering and a stationary pronucleus. Exchange of the wandering

pronuclei
is

conjugant.

followed by the fusion of the two pronuclei in each The synkaryon then divides. One of the two nuclei

formed by
four nuclei

this division degenerates, while the other gives rise to

ferentiated into

by two divisions. The latter presently become diftwo micronuclei and two macronuclei, followed by a cytoplasmic division. The time two conjugants remain paired is said to be 20-38 or more hours (Chen, 1946c). In this Paramecium also, various nuclear activities have been reported. Chen (1940a, c) found that conjugation between a micronucleate and an amicronusometimes occur. In such a case, the micronucleus in the normal individual divides three times, and one of the pronuclei migrates into the amicronucleate in which there is naturally no nuclear division. The single haploid nucleus ("hemicaryon") in each individual divides three times as mentioned above and four nuclei are produced. Thus amicronucleate becomes micronucleated. Conjugating pairs sometimes separate from each other in a few hours. Chen (1946c) found that when such pairs are kept in a depression slide, temporary pairing recurs daily for many days, though there is seemingly no nuclear change. Chen (1940) further observed that the micronucleus in this species is subject to variation in size and
cleate can

190
in the

PROTOZOOLOGY
quantity of chromatin
it

contains, which gives rise to dif-

ferent (about 80 to several hundred)

conjugation in different races, and that polyploidy

chromosome numbers during is not uncomis

mon

in this ciliate.

This investigator considers that polyploidy

more than two pronuclei which he observed on several occasions. The increased number of pronuclei in a conjugant may be due to: (1) the failure of one of the two nuclei produced by the first or second division to degenerate; (2) the conjugation between a unimicronucleate and a bimicronucleate, or (3) the faila result of fusion of

ure of the wandering pronucleus to enter the other conjugant; with

view Wichterman (1946) agrees. Apparently polyploidy occurs in other species also; for example, in P. caudatum (Calkins
this latter

and

Cull, 1907;

Penn, 1937).

In P. trichium, Diller (1948) reported that the usual process of

conjugation

is the sequence of three micronuclear divisions, producing the pronuclei (during which degeneration of nuclei may oc-

self-fertilization

first and second divisions), cross- or and three divisions of the synkarya. Ordinarily four of the eight nuclei become macronuclei, one remains as the micronucleus and the other three degenerate. The micronucleus divides at each of the two cytoplasmic divisions. Exchange of strands of the macronuclear skein may take place between the conjugants. Diller

cur at the end of both the

found a number

of variations

such as omission of the third prefer-

tilization division,

autogamous development, etc., and remarked that heteroploidy is pronounced and common. In P. aurelia possessing typically two micronuclei, the process of conjugation was studied by Maupas (1889), Hertwig (1889), Diller (1936), Sonneborn (1947), etc., and is as follows: Soon after biassociation begins, the two micronuclei in each conjugant divide twice and produce eight nuclei, seven of which degenerate, while the remaining one divides into two gametic nuclei (Maupas, Woodruff, Sonneborn) Diller notes that two or more of the eight nuclei divide for the third time, but all but two degenerate; the two gametic nuclei may or may not be sister nuclei. All agree that there are two functional pronuclei in each conjugant. As in other species of Paramecium already noted, there is a nuclear exchange which results in the formation of a synkaryon in each conjugant. The synkaryon divides twice and the conjugants separate from each other at about this time. Two nuclei develop into macronuclei and the other two
into micronuclei. Prior to the first cytoplasmic division of the excon-

jugant, the micronuclei divide once, but the macronucleus does not
divide, so that each of the

two daughters receives one macronucleus

REPRODUCTION

191

and two micronuclei. The original macronucleus in the conjugant becomes transformed into a skein which breaks up into 20 to 40 small masses. These are resorbed in the cytoplasm as in other species. As to when these nuclear fragments are absorbed, depends upon the nutritive condition of the organism (Sonneborn); namely, under a poor nutritional condition the resorption begins and is completed early, but under a better condition this resorption takes place after
several divisions.

During conjugation reciprocal migration of a pronucleus thus ocall cases. During biassociation and even in autogamy (p. 203), there develops a conical elevation ("paroral cone") and the nuclear migration takes place through this region. Although there is ordinarily no cytoplasmic exchange between the conjugants, this may occur in some cases as observed by Sonneborn (1943a, 1944). P. aurelia of variety 4, according to Sonneborn, do occasionally not separate after fertilization, but remain united by a thin strand in the region of the paroral cones. In some pairs, the strand enlarges into a broad band through which cytoplasm flows from one individual to the other. The first division gives off a normal single animal from each of the "parabiotic twins" and the two clones derived from the two individuals belong to the same mating type (p. 192). Conjugation between different species of Paramecium has been attempted by several workers. Muller (1932) succeeded in producing a few pairings between normal P. caudatum and exconjugant P. multimicronucleatum. The nuclear process ran normally in caudatum, which led Muller to believe that crossing might be possible, but without success. De Garis (1935) mixed "double animals" (p. 228) of P. caudatum and conjugating population of P. aurelia. Pairing between them occurred readily, in which the aurelia mates remained attached to caudatum for five to 12 hours. Four pairs remained together, but aurelia underwent cytolysis on the second day. The separated aurelia from other pairs died after showing "cloudy swelling" on the second or third day after biassociation. The caudatum double-animals on the other hand lived for two to 12 (average six) days during which there was neither growth nor division and finally perished after "hyaline degeneration." No information on nuclear
curs in

behavior in these animals

cies of

is

available. Apparently, the different spe-

Paramecium

are incompatible with one another.

In 1937, Sonneborn discovered that in certain races of P. aurelia, two classes of individuals with respect to "sexual" differentiation and that the members of different classes conjugate with
there are

each other, while the members of each class do not. The members of

192

PROTOZOOLOGY

a class or caryonide (Sonneborn, 1939) are progeny of one of the two individuals formed by the first division of an exconjugant and thus
possess the

same macronuclear

constitution. These classes were des-

ignated by Sonneborn (1938) as mating types. Soon a similar phe-

nomenon was found by

several workers in other species of Para-

#*
A
*~K
'

,r ,*

.-

^
^*%
%

4.

it

_
'

im.

_i .*_,

Fig. 84. Mating behavior of Paramecium bursaria (Jennings), a, individuals of a single mating type; b, 6 minutes after individuals of two mating types have been mixed; c, after about 5 hours, the large masses have

been broken down into small masses;

d, after

24 hours, paired conjugants.

mecium; namely, P. bursaria (Jennings, 1938), P. caudatum (Gilman, 1939; Hiwatashi, 1949-1951), P. trichium, P. calkinsi (Sonneborn, 1938) and P. multimicronucleatum (Giese, 1939). When organisms which belong to different mating types are brought together, they adhere to one another in large clumps ("agglutination") of numerous individuals (Fig. 84, b). After a few to several hours, the

REPRODUCTION
large masses break

193
(c)

down

into small masses

and

still later,

con-

jugants appear in pairs types are definitely

action.

(d).

The only other

ciliate in

which mating

known to occur is Euplotes patella in which, according to Kimball (1939), there occurs no agglutination mating re-

How widely mating types occur is not known at present. But as was pointed out by Jennings, the mating types may be of general occiliates; for example, Maupas (1889) observed that (Loxophyllum) fasciola, Leucophrys patula, Stylonychia pustulata, and Onychodromus grandis, conjugation took place between the members of two clones of different origin, and not among

currence

among

in Lionotus

the
of

members

of a single clone. Precise information

mating types among

different ciliates

on the occurrence depends on future research.

In Paramecium aurelia, Sonneborn distinguishes seven varieties which possess the same morphological characteristics of the species, but which differ in addition to mating types, also in size, division rate, conditions of temperature and light under which mating reaction may occur, etc. (Sonneborn, 1947). There occurs ordinarily no conjugation between the clones of different varieties. Within each of six varieties, there are two mating types, while there is only one type in the seventh variety. Animals belonging to the same variety, but to different mating types, only conjugate when put together (Table G). Under optimum breeding conditions two mating types of the same variety give 95 per cent immediate agglutination and conjugation. But exceptions occur. Sonneborn and Dipell (1946) place the 7 varieties of aurelia under two groups: A (varieties 1, 3, 5 and 7) and B (varieties 2, 4 and 6) on the basis of their conjugational reactions. Mating types in group A do not conjugate with those of group B; no mating type of group B is known to conjugate with any type of other varieties in this group; but a number of combinations of mating types belonging to different varieties of group A conjugate with each other. For example, varieties 1 and 5 conjugate (namely, type I with and type II with type IX); however these interparietal mattype ing reactions are (1) always less intense than intra varietal reaction, (2) dependent upon the degree of reactivity of the culture, and (3) different from the intravarietal reaction with respect to the conditions for optimum reaction. Furthermore in most cases, the progeny of intervarietal matings are not viable. In the varieties of group A, the mating types appear to be of a more general sort. Therefore, Sonneborn (1947) designated even- and odd-numbered types as + and respectively.


194

PROTOZOOLOGY
Table
6.

Groups, varieties and mating types in Paramecium

aurelia

(Sonneborn)

indicates that conjugation does not occur;

numbers show the

maximum

percentage of conjugant-pairs formed; Inc.

indicates incomplete mating reaction

Group


REPRODUCTION
Table
7.

195

Varieties and mating types in Paramecium bursaria (Jennings; Jennings and Opitz; Chen)

+
Variety

indicates that conjugation occurs;

indicates that

it

does not

19G

PROTOZOOLOGY

seemingly normal during the first 16 hours, become abnormal suddenly after that time, and the micronuclei divide only once and there is no nuclear exchange. The death of conjugants or exconjugants is possibly due to physiological incompatibility between the varieties upon coming in contact or probably due to "something that diffuses from one conjugant to the other." Studies of mating types have revealed much information regarding conjugation. Conjugation usually does not occur in well-fed or extremely starved animals, and appears to take place shortly after the depletion of food. Temperature also plays a role in conjugation, as it takes place within a certain range of temperature which varies even in a single species among different varieties (Sonneborn). Light seems to have different effects on conjugation in different varieties of P. aurelia. The time between two conjugations also varies in different species and varieties. In P. bursaria, Jennings found that in some races the second conjugation would
not take place for many months after the first, while in others such an "immature" period may be only a few weeks. In P. aurelia, in some varieties there is no "immature" period, while in others there
is

6 to 10 days' "immaturity."

Very little is known about the physiological state of conjugants compared with vegetative individuals. Several investigators observed that animals which participate in conjugation show much viscous body surface. Boell and Woodruff (1941) found that the mating individuals of Paramecium calkinsi show a lower respiratory rate than not-mating individuals. Neither is the mechanism of conjugation understood at present. Kimball (1942) discovered in Euplotes patella, the fluid taken from cultures of animals of one type
as

induces conjugation

among

the animals of other types

(p.

235). Pre-

sumably certain substances are secreted by the organisms and become diffused in the culture fluid. In Paramecium aurelia, Sonneborn (1943) found that of the four races of variety 4, race 51 was a "killer," while the other three races, "sensitive." Fluid in which the killer race grew, kills the individuals of the sensitive races. As has been mentioned already, P. bursaria designated as type T (variety 5) (Table 7) conjugates with none. But Chen (1945) found that its
culture fluid induces conjugation

among a
2, 3,

small

number
6, in

of the indi-

viduals of one mating type of varieties

which nuclear changes proceed as in normal conjugation. Furthermore, this fluid is capable of inducing autogamy in single animals. Other visible influences of the fluid on organisms are sluggishness of movement and darker coloration and distortion of the body.

4 and

REPRODUCTION

197

Boell and Woodruff (1941) noticed that in P. calkinsi, living indi-

viduals of one mating type will agglutinate with dead ones of the complementary mating type. A similar phenomenon was also observed by Metz (194(5, 1947, 1948) who employed various methods of killing the animals. The pairs composed of living and formaldehydekilled animals, behave much like normal conjugating pairs; there is of course no cross-fertilization, but the living member of the pair undergoes autogamy. While the "mating type substances" can be destroyed by exposure to 52C. for five minutes; by X-irradiation; by exposure of formaldehyde-killed reactive animals to specific antisera or to 100C, etc., Metz demonstrated that animals may be killed by many reagents which do not destroy these substances. Furthermore, all mating activities disappear when the animals are thoroughly broken up, which suggests that Paramecium might release some mating substance inhibitory agent. This agent was later found in this Paramecium (Metz and Butterfield, 1950). Metz (4948) points out that the mating reaction involves substances present on the surfaces of the cilia, and supposes that the interaction between two mating-type substances initiates a chain of reactions leading up to the process of conjugation and autogamy. Hiwatashi (1949a, 1950) using four groups (each composed of two mating types) of P. caudatum, confirmed Metz's observation. Metz and Butterfield (1951) more recently report that non-proteolytic enzymes (lecithinase, hyaluronidase, lysozyme, ptyalin, ribonuclease) have no detectable effect on the mating reactivity of P. calkinsi; but proteolytic enzymes such as trypsin and chymotrypsin destroy the mating reactivity, and mating substance activity was not found in the digest of enzyme-treated organisms. The two observers believe that the mating reactivity is dependent upon protein integrity. When the ciliate possesses more than one micronucleus, the first division ordinarily occurs in all and the second may or may not take place in all, varying apparently even among individuals of the same species. This seems to be the case with the majority, although more than one micronucleus may divide for the third time to produce several pronuclei, for example, two in Euplotes patella, Stylonychia pustulata; two to three in Oxytricha fallax and two to four in Uroleptus mobilis. This third division is often characterized by long extended nuclear membrane stretched between the division products.

Ordinarily the individuals which undergo conjugation appear to

be morphologically similar to those that are engaged in the trophic

activity,

but

in

some

species, the

organism divides just prior to

198

PROTOZOOLOGY

Fig. 85.

The

life-cycle of Nyctotherus cordiformis in

a,

Hyla

versicolor

a cyst; b, excystment in tadpole; c, d, division is repeated until host metamorphoses; e, smaller preconjugant; f-j, conjugation; k, exconjugant; 1, amphinucleus divides into 2 nuclei, one micronucleus and the other passes through the "spireme ball" stage before developing into a macronucleus; k-n, exconjugants found nearly exclusively in recently transformed host; o, mature trophozoite; p-s, binary

(Wichterman).

fission stages;

t,

precystic stage.

REPRODUCTION
conjugation.

199

According to Wichterman (1936), conjugation in 85) takes place only among those which live in the tadpoles undergoing metamorphosis (f-j). The conjugants are said to be much smaller than the ordinary trophozoites, because of the preconjugation fission (d-e). The micronuclear divisions are similar to those that have been described for Paramecium caudatum and finally two pronuclei are formed in each conjugant. Exchange and fusion of pronuclei follow. In each exconjugant, the synkaryon divides once to form the micronucleus and the macronuclear anlage (k-l) which develops into the "spireme ball" and finally into the macronucleus (m-o). A sexual process which is somewhat intermediate between the sexual fusion and conjugation, is noted in several instances. According to Maupas' (1888) classical work on Vorticella nebulifera, the ordinary vegetative form divides twice, forming four small individuals, which become detached from one another and swim about independently. Presently each becomes attached to one side of a stalked individual. In it, the micronucleus divides three times and produces eight nuclei, of which seven degenerate; and the remaining nucleus divides once more. In the stalked form the micronucleus diNyctotherus cordiformis (Fig.
vides twice, forming four nuclei, of which three degenerate,

and the

other dividing into two. During these changes the two conjugants fuse completely. The wandering nucleus of the smaller conjugant
unites with the stationary nucleus of the larger conjugant, the other

two pronuclei degenerating. The synkaryon divides several times to form a number of nuclei, from some of which macronuclei are differentiated and exconjugant undergoes multiplication. In Vorticella

microstoma (Fig. 86), Finley (1943) notes that a vegetative indi-

vidual undergoes unequal division except the micronucleus which

divides equally (a),

and forms a
(b).

large stalked

macroconjugant and a

The conjugation which requires 1824 hours for completion, begins when a microconjugant attaches itself to the lower third of a macroconjugant. The protoplasm of the microconjugant enters the macroconjugant (c). The micronucleus of
small free microconjugant

the microconjugant divides three times, the last one of which being reductional (d, e), while that of the macroconjugant divides twice
(one mitotic and one meiotic). Fusion of one of each produces a synkaryon (/) which divides three times. One of the division products becomes a micronucleus and the other seven macronuclear anlagen (g, h) which are distributed among the progeny (i,j). Another example of this type has been observed in Metopus es

200
(Fig. 87).

PROTOZOOLOGY
According to

No land

(1927), the conjugants fuse along the

and the micronucleus in each individual divides in the same way as was observed in Paramecium caudatum ib-e). But the cytoplasm and both pronuclei of one conjugant pass into the other (J), leaving the degenerating macronucleus and a small
anterior end (a),

ley),

Fig. 86. Sexual reproduction in Vorticella microstoma, X800 (Fina, preconj ligation division which forms a macroconjugant ami a microconjugant; b, a macroconjugant with three microconjugants; c, a microconjugant fusing with a macroconjugant; d, the micronucleus of the microconjugant divided into four nuclei; e, with 12 nuclei formed by divisions of the two micronuclei of conjugants; f, synkaryon; g, eight nuclei after

three divisions of synkaryon; h, seven enlarging macronuclear anlagen and a micronucleus in division; i, first division; j, a daughter individual with a micronucleus, four macronuclear anlagen. and old macronuclear fragments.

REPRODUCTION
amount

201

of cytoplasm behind in the shrunken pellicle of the smaller conjugant which then separates from the other (j). In the larger exconjugant, two pronuclei fuse, and the other two degenerate and disappear (g, h) The synkaryon divides into two nuclei, one of which condenses into the micronucleus and the other grows into the macronucleus (i, k-m). This is followed by the loss of cilia and encystment.
.

While ordinarily two individuals participate

in conjugation, three

Fig. 87. Conjugation of Metopus es (Noland). a, early stage; b, first micronuclear division; c, d, second micronuclear division; e, third micronuclear division; f, migration of pronuclei from one conjugant into the other; g, large conjugant with two pronuclei ready to fuse; h, large conjugant with the synkaryon, degenerating pronuclei and macronucleus; r formed micronucleus and macronucleus i, large exconjugant with newlj j, small exconjugant with degenerating macronucleus; k-m, development
of

two

nuclei, a,

X290;

b-j,

X250, k-m, X590.

202

PROTOZOOLOGY

or four individuals are occasionally involved. For example, conjuga-

was observed in P. caudatum by Stein (1867), (1889) and in Blepharisma vndulans by Giese (1938) and Weisz (1950). Chen (1940b, 1948) made a careful study of such a conjugaion which he found in Paramecium burtion of three animals
Jickeli

(1884),

Maupas

Fig. 88. Conjugation of three individuals in

Paramecium

bursaria,

prophase of the first nuclear division (the individual on right is a member of a race with "several hundred chromosomes," while the other two belong to another race with "about 80 chromosomes") b, anaphase of the third division (each individual contains 2 degenerating nuclei); c, beginning of pronuclear exchange between two anterior animals; d, e, synkaryon formation; f, after the first division of synkaryon, one daughter nucleus undergoing degeneration in all animals.
(Chen),
a, late

X365

REPRODUCTION
saria (Fig. 88).

203
of association
is

He found

that the usual

manner

conjugation between a pair with the third conjugant attached to the posterior part of one of them (a). Nuclear changes occur in all three

and in each, two pronuclei are formed by three divisions But the exchange of the pronuclei takes place only between two anterior conjugants (c-e) and autogamy (see below) occurs in the
individuals,
(c)
.

third individual.

Fig. 89.
a,

Diagram

illustrating

autogamy

in

Paramecium

aurelia (Diller).

micronuclear division; c, second micronuclear division; d, individual with 8 micronuclei and macronucleus preparing for skein formation; e, two micronuclei dividing for the third time; f, two gamete-nuclei formed by the third division in the paroral cone; g, fusion of the nuclei, producing synkaryon; h, i, first and second division of synkaryon; j, with 4 nuclei, 2 becoming macronuclei and the other 2 remaining as micronuclei; k, macronuclei developing, micronuclei dividing; 1, one of the daughter individuals produced by fission.

normal animal;

b, first

Automixis. In certain Protozoa, the fusion occurs between two which originate in a single nucleus of an individual. This process has been called automixis by Hartmann, in contrast to the
nuclei

amphimixis (Weismann) which

originating in

is the complete fusion of two nuclei two individuals, as was discussed in the preceding pages. If the two nuclei which undergo a complete fusion are present in a single cell, the process is called autogamy, but, if they are in two

204
different cells, then

PROTOZOOLOGY
paedogamy. The autogamy is of common occurThe young sporoplasm contains

rence in the myxosporidian spores.

two nuclei which fuse together

ple in

prior to or during the process of germination in the alimentary canal of a specific host fish, as for exam-

Sphaeromyxa sabrazesi

(Figs. 276; 277)

stomi (Fig. 275). In the Microsporidia,

as in Thelohania legeri (Fig. 76).
Diller (1936) observed in solitary

and Myxosoma catoautogamy appears to initiate

the spore-formation at the end of schizogonic activity of individuals

Paramecium

aurelia (Fig. 89),

micronuclear changes similar to those which occur in conjugating individuals. The two micronuclei divide twice, formcertain

ing eight nuclei (a-d), some of which divide for the third time (e), producing two functional and several degenerating nuclei (/). The two functional nuclei then fuse in the "paroral cone" and form the

synkaryon (g, h) which divides twice into four (i, j). The original macronucleus undergoes fragmentation and becomes absorbed in the cytoplasm. Of the four micronuclei, two transform into the new macronuclei and two remain as micronuclei (k) each dividing into two after the body divided into two (Z). Another sexual process appears to have been observed by Diller (1934) in conjugating Paramecium trichium in which there was no nuclear exchange between the two conjugants. Wichterman (1940) observed a similar process in P. caudatum and named it cytogamy. Two small (about 200/x long) individuals of P. caudatum fuse on their oral surfaces. There occur three micronuclear divisions as in the case of conjugation, but there is no nuclear exchange between the members of the pair. The two gametic nuclei in each individual are said to fuse and form a synkaryon as in autogamy. Sonneborn (1941) finds the frequency of cytogamy in P. aurelia to be correlated with temperature. At 17C, conjugation occurs in about 95 per cent of the pairs and cytogamy in about 5 per cent; but at 10 and 27C, cytogamy takes place in 47 and 60 per cent respectively. In addition, there is some indication that sodium decreases and calcium increases the frequency of occurrence of cytogamy. The paedogamy occurs in at least two species of Myxosporidia, namely, Leptotheca ohlmacheri (Fig. 279) and Unicapsula muscularis (Fig. 280). The spores of these myxosporidians contain two uninucleate sporoplasms which are independent at first, but prior to emergence from the spore, they undergo a complete fusion to metamorphose into a uninucleate amoebula. Perhaps the classical example of the paedogamy is that which was found by Hertwig (1898) in Actinosphaerium eichhorni. The organism encysts and the body di-

REPRODUCTION
vides into

205

numerous uninucleate secondary cysts. Each secondary cyst divides into two and remains together within a common cystwall. In each the nucleus divides twice, and forms four nuclei, one of
which remains functional, the remaining three degenerating. The paedogamy results in formation of a zygote in place of a secondary cyst. Belaf (1923) observed a similar process in Actinophrys sol (Fig. 90). This heliozoan withdraws its axopodia and divides into two uninucleate bodies which become surrounded by a common

Fig. 90.

Paedogamy
c,

in Actinophrys sol,

of axopodia; b,

division into

X460 (Belaf). a, withdrawal two uninucleate bodies, surrounded by

a common gelatinous envelope; d-f, the first reduction division; g-i, the second reduction division; j-1, synkaryon formation.

gelatinous envelope.
clei,

Both

nuclei divide twice

and produce four nu-

three of which degenerate.

haploid nucleus,

The two daughter cells, each with one undergo paedogamy and the resulting individual

now

contains a diploid nucleus. In Paramecium aurelia, Diller (1936) found simple fragmentation of the macronucleus which was not correlated with any special micronuclear activity and which could not be stages in conjugation
if conjugation or autogamy is to new nuclear complex, as is generally held, it is conceivable somewhat the same result might be achieved by "purification

or autogamy. Diller suggests that create a

that

act" (through fragmentation) on the part of the macronucleus

itself,

206

PROTOZOOLOGY
He
coined the term hemixis for this

without involving micronuclei.

reorganization.

Meiosis. In the foregoing sections, references have been

jugation. In
all

made

to

the divisions which the nuclei undergo prior to sexual fusion or con-

Metazoa, during the development

of the

gametes,

the gametocytes undergo reduction division or meiosis, by which the

number of chromosomes is halved; that is to say, each fully mature gamete possesses half (haploid) number of chromosomes typical of
the species (diploid). In the zygote, the diploid
lished.

number

is

reestab-

In the Protozoa in which sexual reproduction occurs during their life-cycle, meiosis presumably takes place to maintain the constancy of chromosome-number, but the process is understood only
in

a small number of species.

Fig. 91. Mitotic and meiotic micronuclear divisions in conjugating Didinium nasutum. (Prandtl, modified), a, normal micronucleus;b, equatorial plate in the first (mitotic) division; c, anaphase in the first division; d, equatorial plate in the second division; e, anaphase in the second
(meiotic) division.

In conjugation, the meiosis seems to take place in the second micronuclear division, although in some, for example, Oxytricha fallax, according to Gregory, the actual reduction occurs during the a reduction in first division. Prandtl (1906) was the first to note
in the Protozoa. In conjugating Didinium he observed 16 chromosomes in each of the daughter micronuclei during the first division, but only 8 in the second division. Since that time, the fact that meiosis occurs during the second micronuclear division has been observed in Chilodonella uncinata (Enrique; MacDougall), Carchesium polypinum (Popoff), Uroleptus halseyi (Calkins), etc. (note the ciliates in Table 5 on p.

number

of

chromosomes

nasutum

(Fig. 91),

168). In various species of

number
(p.

of

Paramecium and many other forms, the chromosomes appears to be too great to allow a precise

counting, but the observations of Sonneborn, as quoted elsewhere

234) and of Jennings (1942) on P. aurelia and P. bursaria respec-

REPRODUCTION

207

tively, indicate clearly the occurrence of meiosis prior to nuclear ex-

change during conjugation. Information on the meiosis involved in the complete fusion of gametes is even more scanty and fragmentary. In Monocystis rostrata (Fig. 92), a parasite of the earthworm, Mulsow (1911) noticed that

'

^^V

^tzm&j^

w
h-j,

-m

Fig. 92. Mitosis and meiosis in Monocystis rostrata (Mulsow). a-g, mitosis; h-j, meiosis. a, a resting nucleus in the gametocyte; b, development of chromosomes; c, polar view of equatorial plate; d, longitudinal splitting of eight chromosomes; e, separation of chromosomes in two groups; f, late anaphase; g, two daughter nuclei; h, i, polar view of the equatorial plate in the last division; j, anaphase, the gamete nucleus is

now

haploid

(4). a-c,

X1840; d-g, X1400;

X3000.

the nuclei of two gametocytes which encyst together, multiply by mitosis in which eight chromosomes are constantly present (a-g),
receives only 4

gamete formation, each daughter nucleus chromosomes (h-j). In another species of Monocystis, Calkins and Bowling (1926) observed that the diploid number of chromosomes was 10 and that haploid condition is established in the last gametic division thus confirming Mulsow's finding. In the paedogamy of Actinophrys sol (Fig. 90), Belaf (1923) finds 44 chromosomes in the first nuclear division, but after two meiotic divisions, the remaining functional nucleus contains only 22 chromosomes so that when paedogamy is completed the diploid number is restored. In Polytoma uvella, Moewus finds each of the two gametes is haploid (8 chromosomes) and the zygotes are diploid. The synkaryon divides twice, and during the first division reduction division
but in the
last division in

takes place.

208

PROTOZOOLOGY

In the coccidian, Aggregata eberthi (Fig. 246), according to Dobell and Belaf (1926) and in the gregarine, Diplocystis schneideri, according to Jameson (1920), there is no reduction
(1925), Naville (1925)
in

the

number

of

first

zygotic division

chromosomes during the gamete-formation, but the is meiotic, 12 to 6 and 6 to 3, respectively. A

similar reduction takes place also in Actinocephalus parvus (8 to 4,

Weschenf elder, 1938), Greg arina blattarum (6 to 3, after Sprague, Hauschka, 1943), etc. Trichonympha and other flagellates (p. 185) of woodroach, Polytoma
after

1941), Adelina deronis (20 to 10, after

Fig. 93. Degeneration or aging in Stylonychia pustulata. X340 (Maupas, modified), a, Beginning stage with reduction in size and completely atrophied micronucleus; b, c, advanced stages in which disappearance of the frontal zone, reduction in size, and fragmentation of the macronucleus occurred; d, final stage before disintegration.

and Chlamydomonas (p. 276) also undergo postzygotic meiosis. Thus in these organisms, the zygote is the only stage in which the
nucleus
is

diploid.

years ago Weismann pointed out that a protozoan grows and muliplies by binary fission or budding into two equal or unequal individuals without loss of any protoplasmic part and these in turn grow and divide, and that thus in Protozoa there is neither senescence nor natural death which occur invariably in Metazoa in which germ and soma cells are differentiated. Since that time, the problem of potential immortality of Protozoa has been a matter which attracted the attention of numerous investigators. Because of large dimensions, rapid growth and reproduction, and ease with

Some seventy

REPRODUCTION

209

which they can be cultivated in the laboratory, the majorhVy of Protozoa used in the study of the problem have been free-living freshwater ciliates that feed on bacteria and other microorganisms. The very first extended study was made by Maupas (1888) who isolated Stylonychia pustulata on February 27, 1886, and observed 316 binary fissions until July 10. During this period, there was noted a gradual decrease in size and increasing abnormality in form and structure, until the animals could no longer divide and died (Fig. 93). A large number of isolation culture experiments have since been
carried on

numerous

species of ciliates

results obtained are not in agreement.

by many investigators. The However, the bulk of ob-

tained data indicates that the vitality of animals decreases with the

passing of generations until finally the organisms suffer inevitable

death, and that in the species in which conjugation or other sexual

reproduction occurs, the declining vitality often becomes restored. Perhaps the most thorough experiment was carried on by Calkins
(1919, 1933) with Uroleptus mobilis. Starting with

November

17, 1917, a series of pure-line cultures

an exconjugant on was established by

the daily isolation method. It was found that no series lived longer

than a year, but when two of the progeny of a series were allowed to conjugate after the first 75 generations, the exconjugants repeated the history of the parent series, and did not die when the parent series died. In this way, lines of the same organism have lived for more than 12 years, passing through numerous series. In a series, the average division for the first 60 days was 15.4 divisions per 10
days, but the rate gradually declined until death. Woodruff

and

Spencer (1924) also found the isolation cultures of Spathidium spathula (fed on Colpidium colpoda) died after a gradual decline in the division rate, but were inclined to think that improper environmental conditions rather than internal factors were responsible for
the decline.

On the other hand, Woodruff (1932) found that 5071 generations produced by binary fission from a single individual of Paramecium aurelia between May 1, 1907 and May 1, 1915, did not manifest any decrease in vitality after eight years of continued asexual reproduction. Other examples of longevity of ciliates without conjugation are: Glaucoma for 2701 generations (Enriques, 1916), Paramecium caudatum for 3967 generations (Metalnikov, 1922), Spathidium spathula for 1080 generations (Woodruff and Moore, 1924), Didinium nasutum for 1384 generations (Beers, 1929), etc. With Actinophrys sol, Belaf (1924) carried on isolation cultures for 1244 generations for a period of 32 months and noticed no decline in the division rate.

210

PROTOZOOLOGY
made

a similar observation on Eudorina (1921) It would appear that in these forms, the life continues indefinitely

Hartmann

without apparent decrease in vital activity. As has been noted in the beginning part of the chapter, the macronucleus in the ciliates undergoes, at the time of binary fission a reorganization process before dividing into two parts and undoubtedly, there occurs at the same time extensive cytoplasmic reorganization as judged by the degeneration and absorption of the old, and formation of the new, organellae. It is reasonable to suppose that this reorganization of the whole body structure at the time of division is an elimination process of waste material accumulated by the organism during the various phases of vital activities as was con-

by Kidder and others (p. 150) and that this elimination, though not complete, enables the protoplasm of the products of division to carry on their metabolic functions more actively. As the generations are multiplied, the general decline in vitality
sidered
is

manifest not only in the decreased division-rate, slow growth,

of certain organellae, etc.,

abnormal form and function

but also

in

inability to complete the process involved in conjugation. Jennings

(1944) distinguished four successive periods in various clone cultures

Paramecium bursaria; namely, (1) a period of sexual immaturity during which neither sexual reaction nor conjugation occurs; (2) a period of transition during which weak sexual reactions appear in a
of

few individuals;
place readily
(4)

(3)

a period of maturity in which conjugation takes

are brought together; and
first

when proper mating types

a period of decline, ending in death. The length of the

two

periods depends on the cultural conditions. Exconjugant clones that

are kept in condition under which the animals multiply rapidly,

reach maturity in three to five months, while those subjected to depressing condition require 10 to 14
third period lasts for several years

period during which fission

months to reach maturity. The and is followed by the fourth becomes slower, abnormalities appear,
Paramecium

many

individuals die and the clones die out completely.

affect the longevity of clones in

Does conjugation
busaria?

comparative study of the fate of exconjugants and nonconjugants led Jennings (1944a) to conclude that (1) conjugation results in production of one of the following four types: (a) exconjugants perish without division, (b) exconjugants divide one to four times and then die, (c) exconjugants produce weak abnormal clones which may become numerous, and (d) exconjugants multiply vigorously and later undergo conjugation again; at times the latter are

REPRODUCTION

211

more vigorous than the parent clones, thus showing rejuvenescence through conjugation; (2) conjugation of young clones results in little or no mortality, while that of old clones results in high (often 100 per cent) mortality; (3) conjugation between a young and an old clone, results in the death of most or all of the exconjugants; (4) the two members of a conjugating pair have the same fate; and (5) what other causes besides age bring about the death, weakness or abnormality of the exconjugants, are not known. It is probable that the process of replacing old macronuclei by micronuclear material which are derived from the products of fusion of two micronuclei of either the same (autogamy) or two different animals (conjugation), would perhaps result in a complete elimination of waste substances from the newly formed macronuclei, and divisions which follow this fusion may result in shifting the waste substances unequally among different daughter individuals. Thus in some individuals there may be a complete elimination of waste material and consequently a restored high vitality, while in others the influence of waste substances present in the cytoplasm may offset or handicap the activity of new macronuclei, giving rise to stocks of low vitality which will perish sooner or later. In addition in conjugation, the union of two haploid micronuclei produces diverse genetic constitutions which would be manifest in progeny in manifold ways. Experimental evidences indicate clearly such is actually the
case.

In

many

ciliates,

the elimination of waste substances at the time

of binary fission

and sexual reproduction (conjugation, and autog-

amy), seemingly allow the organisms continued existence through a long chain of generations indefinitely. Jennings (1929, 1942) who reviewed the whole problem states: "Some Protozoa are so constituted that they are predestined to decline and death after a

number of generations. Some

but this
is

are so constituted that decline occurs,

checked or reversed by substitution of reserve parts for those that are exhausted; they can live indefinitely, but are dependent on this substitution. In some the constitution is such that life and multiplication can continue indefinitely without visible substitution of a reserve nucleus for an exhausted one; but whether this is due to the continued substitution, on a minute scale, of reserve parts for those that are outworn cannot now be positively stated. This perfected condition, in which living itself includes continuously the necessary processes of repair and elimination,
in
is

found

some

free cells,

but not in

all."

212

PROTOZOOLOGY
Regeneration
parts,
all

The capacity of regenerating the lost among different species, is characteristic of

servations of
fact that

though variable Protozoa from simple

forms to those with highly complex organizations, as shown by ob-

numerous investigators. It is now a well established when a protozoan is cut into two parts and the parts are

kept under proper environmental conditions, the enucleated portion is able to carry on catabolic activities, but unable to undertake anabolic activities,

and consequently degenerates sooner or

later.

Brandt

(1877) studied regeneration in Actinosphaerium eichhorni and found that only nucleate portions containing at least one nucleus regener-

ated and enucleate portions or isolated nuclei degenerated. Similarly Gruber (1886) found in Amoeba proteus the nucleate portion regenerin a

ated completely, while enucleate part became rounded and perished few days. The parts which do not contain nuclear material may continue to show certain metabolic activities such as locomotion,
contraction of contractile vacuoles,
etc., for

some time;

for example,

Grosse-Allermann (1909) saw enucleate portions of Amoeba verrucosa alive for 20 to 25 days, while Stole (1910) found enucleate Amoeba proteus living for 30 days. Clark (1942, 1943) showed that Amoeba proteus lives for about seven days after it has been deprived of its nucleus. Enucleated individuals show a 70 per cent depression of respiration and are unable to digest food due to the failure of zymogens to be activated in the dedifferentiating cytoplasm. According to Brachet (1950), the enucleated half of an amoeba shows a steady
decrease in ribonucleic acid content, while the nucleated half retains a much larger amount of this substance. Thus it appears that the
synthesis of the cytoplasmic particles containing ribonucleic acid
is

under the control of the nucleus. In Arcella (Martini; Hegner) and Difflugia (Verworn; Penarcl), when the tests are partially destroyed, the broken tests remain unchanged. Verworn considered that in these testaceans test-forming activity of the nucleus is limited to the time of asexual reproduction of the organisms. On the other hand several observers report in Foraminifera the broken shell is completely regenerated at all times. Verworn pointed out that this indicates that here the nucleus controls the

formation of shell at

all

times. In a radiolarian, Thalassi-

colla nucleata, the central capsule,

if dissected out from the rest of body, will regenerate into a complete organism (Schneider). A few regeneration studies on Sporozoa have not given any results to be considered here, because of the difficulties in finding suitable media

for cultivation in vitro.

REPRODUCTION
An enormous number
of regeneration
ciliates
is

213

experiments have been coninvestigators.

is

ducted on more than 50

generation. In

by numerous

Here

also the general conclusion

that the nucleus

necessary for re-

essential nucleus for regeneration, as

macronucleus seems to be the only judged by the continued division on record of several amicronucleate ciliates and by experiments such as Schwartz's in which there was no regeneration in Stentor coeruleus from which the whole macronucleus had been removed. A remarkably small part of a protozoan is known to be able to regenerate completely if nuclear material is included. For example, Sokoloff found 1/53-1/69 of Spirostomum ambiguum and 1/70-1/75 of Dileptus anser regenerated and Phelps showed portions down to 1/80 of an amoeba were able to regenerate. In Stentor coeruleus, pieces as small as 1/27 (Lilly) or 1/64 (Morgan) of the original specimens or about 70/jl in diameter (Weisz) regenerate. Burnside cut 27 specimens of this ciliate belonging to a single clone, into two or more parts in such a way that some of the pieces contained a large portion of the nucleus while others a small portion. These fragments regenerated and multiplied, giving rise to 268 individuals. No dimensional differences resulted from the different amounts of nuclear material present in the cut specimens. Apparently regulatory processes took place and in all cases normal size was restored, recases, the

many

gardless of the

amount

of the nuclear material in ancestral pieces.

Thus biotypes
ties in

of diverse sizes are

not produced by causing inequali-

the proportions of nuclear material in different individuals.

In addition to these restorative regenerations, there are physiological regenerations in

which as

in the case of asexual

cilia,

and sexual

re-

production, various organellae such as

flagella,

cytostome,
is

contractile vacuoles, etc., are completely regenerated. Information

now

available on the process of morphogenesis in regeneration and

reorganization in certain ciliates (Chatton and Lwoff, 1935; Bala-

muth, 1940; Summers, 1941; Faure-Fremiet, 1948; Weisz, 1948,

1951).

References

Balamuth, W.

(1940) Regeneration in Protozoa: a problem of morphogenesis. Quart. Rev. Biol., 15:290. (1951) Biological studies on Entamoeba histolytica. III. J. Infect. Dis., 88:230. Barker, H. A. and Taylor, C. V.: (1931) A study of the conditions of encystment of Colpoda cucullus. Physiol. Zool., 4:620. (1933) Studies on the excystment of Colpoda cucullus. Ibid., 6:127.
:

214

PROTOZOOLOGY

Beers, C. D.: (1926) The life-cycle in the ciliate Didinium nasutum with reference to encystment. J. Morphol., 42:1. (1927) Factors involved in encystment in the ciliate Didinium nasvtum. J. Morphol. Physiol., 43:499. (1928) Rhythms in Infusoria with special reference to Didinium nasutum. J. Exper. Zool., 51:485.
(1930)
(1931)
ciliate, etc.

On the possibility of Am. Nat., 63:125.

indefinite

reproduction in the

nasutum.

effects of conjugation in the ciliate Didinium Exper. Zool., 58:455. (1935) Structural changes during encystment and excystment in the ciliate Didinium nasutum. Arch. Protist., 84:133. (1937) The viability of 10-year old Didinium cysts. Am. Nat., 71:521. (1945) Some factors affecting excystment in the ciliate TilJ.

Some

Una magna.
(1945a)

Physiol. Zool., 18:82. process in the ciliate Didinium nasutum. J. El. Mitchell Sc. Soc, 61 264. (1946) History of the nuclei of Tillina magna during division

The excystment

special reference to the role of bacteria. J. Exper. Zool., 103:201. (1946b) Tillina magna: micronuclear number, etc. Biol. Bull., 91:256. (1947) The relation of density of population to encystment
:

and encystment. J. Morphol., 78:181. (1946a) The excystment in Didinium nasutum with

in Didinium nasutum. J. El. Mitchell Sc. Soc, 63:141. Belar, K. (1921) Untersuchungen ueber Thecamoeben der Chlamydophrys-Gruppe. Arch. Protist., 43:287. (1923) Untersuchungen an Actinophrys sol. I. Ibid., 46: 1.

(1924) II. Ibid., 48:371. (1926) Der Formwechsel der Protistenkerne. Ergebn. u. Fortsch. Zool., 6:235. Bodine, J. H.: (1923) Excystation of Colpoda cucullus. J. Exper.
Zool., 37:115.

Boell, E. J. and Woodruff, L. L.: (1941) Respiratory metabolism of mating types in Paramecium calkinsi. J. Exper. Zool., 87:385. Brachet, J.: (1950) Un etude cytochimique des fragments nuclees
et enuclees d'amibes. Experientia, 6:294.
v. (1922) Ueber eine neue Strombidium-Art aus Heligoland. Arch. Protist., 45:129. Butschli, O.: (1876) Studien liber die ersten Entwicklungsvorgange der Eizelle, die Zelltheilung und die Conjugation der Infusorien. Abh. Senk. Nat. Ges. Frankf., 10:1. Btjrnside, L. H.: (1929) Relation of body size to nuclear size in Stentor coeruleus. J. Exper. Zool., 54:473. Burt, R. L., Kidder, G. W. and Claff, C. L.: (1941) Nuclear reorganization in the family Colpodidae. J. Morphol., 69:537. Calkins, G. N.: (1919) Uroleptus mobilis. II. J. Exper. Zool., 29:
:

Buddenbrock. W.

121.

(1933)

The

biology of the Protozoa. 2nd ed. Philadelphia.

REPRODUCTION

215

and Bowling, C: and Cull, W.

R.
Biol. Bull., 51:385.
:

(1926) Gametic meiosis in Monocystis.

S. (1907) The conjugation of Paramecium aurelia (caudatum). Arch. Protist., 10:375. and Summers, F. M.: (editors) (1941) Protozoa in biological research. New York.

Chalkley, H. W.
"peripheral

(1936) The behavior of the karyosome and the chromatin" during mitosis and interkinesis in Amoeba proteus, etc. J. Morphol., 60:13. and Daniel, G. E.: (1933) The relation between the form of
:

the living

cell

and the nuclear phases

of division in

Amoeba
I.

proteus. Physiol. Zool., 6:592.

Chatton, E. and Lwoff,

A.: (1935) Les Cilies Apostomes.

Arch.

zool. exper. gen., 77:1.

Chen, T.

T.: (1936) Observations on mitosis in opalinids. I. Proc. Nat. Acad. Sc, 22:594. (1940) Polyploidy and its origin in Paramecium. J. Hered., 31:175. (1940a) Conjugation in Paramecium bursaria between animals with diverse nuclear constitutions. Ibid., 31:185. (1940b) Conjugation of three animals in Paramecium bursaria. Proc. Nat. Acad. Sc, 26:231. (1940c) Conjugation in Paramecium bursaria between animals with very different chromosome numbers, etc. Ibid., 26:
243. (1945) Induction of conjugation in
Ibid., 31:404.

Paramecium

bursaria, etc.

(1946) Conjugation in Paramecium bursaria. I. J. Morphol., 78:353. (1946a) II. Ibid., 79:125. (1946b) Varieties and mating types in Paramecium bursaria. I. Proc. Nat. Acad. Sc, 32:173. (1946c) Temporary pair formation in Paramecium bursaria. Biol. Bull., 91:112. (1948) Chromosomes in Opalinidae, etc J. Morphol., 83:
281.

Clark, A. M.: (1942) Some effects of removing the nucleus from Amoeba. Australian J. Exper. Biol., 20:241.
(1943)

Some
:

physiological

functions

of

the

nucleus

in

Amoeba, etc. Ibid., 21:215. Cleveland, L. R. (1938) Longitudinal and transverse division in two closely related flagellates. Biol. Bull., 74:1. (1938a) Origin and development of the achromatic figure.
Ibid., 74:41.

(1949) The whole life cycle of chromosomes and their coiling systems. Tr. Am. Philos. Soc, 39:1. (1949a) Hormone-induced sexual cycles of flagellates. J. Morphol., 85:197. (1950) II. Ibid., 86:185. - (1950a) III. Ibid., 86:215.

216

PROTOZOOLOGY

(1950b) IV. Ibid., 87:317. (1950c) V. Ibid., 87:349. (1951) VI. Ibid., 88:199. (1951a) VII. Ibid., 88:385. Hall, S. R., Sanders, E. P. and Collier, J.: (1934) The wood-feeding roach Cryptocercus, etc. Mem. Am. Acad. Arts & Sc., 17:185. Crump, Lettice M.: (1950) The influence of bacterial environment on the excystment of amoebae from soil. J. Gen. Microbiol., 4:
16.

Cutler, D. W. and Crump, L. M.: (1935) The effect of bacterial products on amoebic growth. Brit. J. Exper. Biol., 12:52. Daniel, G. E. and Chalkley, H. W. (1932) The influence of temperature upon the process of division in Amoeba proteus. J. Cell.
:

Comp. Physiol., 2:311. Darby, H. PL: (1929) The effect

of the

hydrogen-ion concentration

on the sequence of protozoan forms. Arch. Protist., 65: 1. Dass, C. M. S.: (1950) Chromatin elimination in Glaucoma pyriformis. Nature, 165:693. Davis, T. G.: (1941) Morphology and division in Tetratoxum unifasciculatum. Tr. Am. Micr. Soc, 60:441. Dawson, J. A.: (1919) An experimental study of an amicronucleate Oxytricha. I. J. Exper. Zool., 29:473. and Hewitt, D. C: (1931) The longevity of encysted Col-

poda.

Am.

Nat., 65:181.

vitality of certain infusorian cysts. Ibid., 63:476. of conjugation between Garis, C. F.: (1935) Lethal effects Paramecium aurelia and double-monsters of P. caudatum. Am. Nat., 69:87. Diller, W. F.: (1936) Nuclear reorganization processes in Paramecium aurelia, etc. J. Morphol., 59:11. (1948) Nuclear behavior of Paramecium trichium during conjugation. Ibid., 82:1. (1950) An extra postzygotic nuclear division in Paramecium caudatum. Tr. Am. Micr. Soc, 69:309. (1950a) Cytological eivdence for pronuclear interchange in Paramecium caudatum. Ibid., 69:317. Dobell, C. (1908) The structure and life history of Copromonas subtilis, etc. Quart. J. Micr. Sc, 52:75. (1917) On Oxnerella maritima, etc. Ibid., 62:515. (1925) The life history and chromosome cycle of Aggregata eberthi. Parasitology, 17:1. (1928) Researches on the intestinal Protozoa of monkeys and man. I, II. Ibid., 20:357. and Laidlaw, P. P.: (1926) On the cultivation of Entamoeba histolytica, etc. Ibid., 18:283. Enriques, P.: (1916) Duemila cinquecento generazioni in un infusorio, senza conjugazione ne partenogenesi, ne depressioni. Rev. Acad. Sc. Bologna, 20:67.

and Mitchell, W. H.: (1929) The

De

REPRODUCTION
Ceratien. Arch. Protist., 51:131. Martha G.: (1950) The
etc. J. Parasit.,

217

Entz, G.: (1925) Ueber Cysten und Encystierung der Siisswasser-

Everritt,

relationship

of

population

growth,
chez

36:586.

Faure-Fremiet,

E.: (1948) Les mecanismes de la morphogenese 3:25. method for inducing conjugation within Finley, H. E.: (1936) Vorticella cultures. Tr. Am. Micr. Soc, 55:323. (1943) The conjugation of Vorticella microstoma. Ibid., 62: 97. Frosch, P.: (1897) Zur Frage der Reinzuchtung der Amoeben. Zentralbl. Bakt. I. Abt., 21:926. Garnjobst, L.: (1928) Induced encystment and excystment in Ewplotes taylori, etc. Physiol. Zool., 1:561. Giese, A. C.: (1938) Size and conjugation in Blepharisma. Arch.
les cilies. Folia Bioth.,

Protist., 91:125.

(1939) Studies on conjugation in Paramecium multimicronucleatum. Am. Nat., 73:432. (1939a) Mating types in Paramecium caudatum. Am. Nat., 73:445. Gilman, L. C.: (1941) Mating types in diverse races of Paramecium caudatum. Biol. Bull., 80:384. Grasse, P.-P.: (1952) Traite de Zoologie. I. Fasc. 1. Paris. Guilcher, Yvette: (1950) Contribution a l'etude des cilies gemmipares, etc. Univ. de Paris thesis, Ser. A. no. 2369. Haagen-Smit, A. J. and Thimann, K. V.: (1938) The excystment of Colpoda cucullus. I. J. Cell. Comp. Physiol., 11:389. Hall, R. P.: (1923) Morphology and binary fission of Menoidium incurvum. Univ. California Publ. Zool., 20:447. (1937) A note on behavior of the chromosomes in Euglena. Tr. Am. Micr. Soc, 56:288. Hartmann, M.: (1917) Ueber die dauernde rein agame Zuchtung von Eudorina elegans, etc. Ber. preuss. Akad. Wiss., Phys.-

Math. Kl., p. Hauschka, T. S.:

760. (1943) Life history and chromosome cycle of the coccidian, Adelina deronis. J. Morphol., 73:529. Hertwig, R.: (1889) Ueber die Conjugation der Infusorien. Abh. bayerl. Akad. Wiss., 17:151. Hinshaw, H. C: (1926) On the morphology and mitosis of Trichomonas buccalis. Univ. California Publ. Zool., 29:159.

Hiwatashi, K.: (1949) Studies on the conjugation of Paramecium, caudatum. I. Sc. Rep. Tohoku Univ. Ser. IV, 18:137.
(1949a) II. Ibid., 18:141. (1950) III. Ibid., 18:270. (1951) IV. Ibid., 19:95. Horvath, J.: (1950) Vitalitatsausserung einer mikronucleuslose Bodenziliate in der vegetativen Fortpflanzung. Oesterr. zool. Ztschr., 2:336. Ilowaisky, S. A.: (1926) Material zum Studium der Cysten der Hypotrichen. Arch. Protist., 54:92.

218

PROTOZOOLOGY
M. (1934) Ueber die Ruhestadienbildung und die damit am Kernapparate verbundenen Veranderungen bei Lionotus cygnus.
:

Ivanic,

Zool.Anz., 108:17.
(1938) Ueber die mit der Chromosomenbildung verbundene promitotische Grosskernteilung bei den Vermehrungsruhe Statien von Chilodon uncinatus. Arch. Protist., 91:61. Jameson, A. P.: (1920) The chromosome cycle of gregarines with special reference to Diplocystis schneideri. Quart. J. Micr. Sc, 64:207. Jennings, H. S.: (1929) Genetics of the Protozoa. Bibliogr. Gen., 5:
105. (1938)

cium

Sex relation types and their inheritance in Paramebursaria. I. Proc. Nat. Acad. Sc, 24:112. (1939) Genetics of Paramecium bursaria. I. Genetics, 24:202. (1941) II. Proc. Am. Philos. Soc, 85:25. (1942) III. Genetics, 27:193. (1942a) Senescence and death in Protozoa and invertebrates. E. V. Cowdry's Problems of ageing. 2 ed. Baltimore. (1944) Paramecium bursaria: Life history. I. Biol. Bull., 86: 131. (1944a) II. J. Exper. Zool., 96:17. and Opitz, Pauline: (1944) Genetics of Paramecium bursaria. IV. Genetics, 29:576.

Raffel, D., Lynch, R. S. and Sonneborn, T. M.: (1932) diverse biotypes produced by conjugation within a clone of Paramecium aurelia. J. Exper. Zool., 62:363. Jickeli, C. F.: (1884) Ueber die Kernverhaltnisse der Infusorien.

The

Zool. Anz., 7:491.

Johnson, W. H. and Evans, F. R.: (1940) Environmental factors affecting encystment in Woodruffia metabolica. Physiol. Zool.,
13:102.
further study of environmental factors af(1941) fecting cystment in Woodruffia metabolica. Ibid., 14:227.
J. M. and Burroughs, R. D.: (1926) The cause and nature encystment in Polyiomella citri. Biol. Bull., 50:38. Kay, M. M.: (1946) Studies on Oxytricha bifaria. III. Tr. Am. Micr. Soc, 65:132. Kidder, G. W. (1933) Studies on Conchophthirus mytili de Morgan.

Kater,
of

Arch. Protist., 79:1. (1938) Nuclear reorganization without cell division in Paraclevelandia simplex, etc. Ibid., 91:69. and Claff, C. L.: (1938) Cytological investigations of Golpoda cucullus. Biol. Bull., 74:178. and Diller, W. F. (1934) Observations on the binary fission of four species of common free-living ciliates, etc Ibid., 67:201.
I.
:

and Stuart, C. A.: (1939) Growth studies on ciliates. II. Physiol. Zool., 12:341. and Summers, F. M.: (1935) Taxonomic and cytological studies on the ciliates associated with the amphipod family, etc. Biol. Bull, 68:51.

REPRODUCTION
Kimball, R.

219

F.: (1939) Change of mating type during vegetative reproduction in Paramecium aurelia. J. Exper. Zool., 81:165. (1939a) Mating types in Euplotes. Amer. Nat., 73:451. (1941) The inheritance of mating type in the ciliate protozoan Euplotes patella. Genetics, 26:158. (1941a) Double animals and amicronucleate animals, etc. J. Exper. Zool., 86:1. (1942) The nature and inheritance of mating types in Euplotes patella. Genetics, 27:269. (1943) Mating types in the ciliate Protozoa. Quart. Rev. Biol., 18:30. Koffman, M.: (1924) Ueber die Bedeutung der Wasserstoffionenkonzentration fur die Encystierung bei einigen Ciliatenarten. Arch. mikr. Anat., 103:168. Kofoid, C. A. and Swezy, Olive: (1919) Studies on the parasites of the termites. I. Univ. California Publ. Zool., 20:1. (1919a) III. Ibid., 20:41. Korschelt, E.: (1927) Regeneration und Transplantation. Vol. 1.

Berlin.

Kudo, R. R.

(1926) Observation on Endamoeba blattae. Am. J. Hyg., 6:139. (1926a) Observations on Lophomonas blattarum, etc. Arch. Protist., 53:191. (1926b) A cytological study of Lophomonas striata. Ibid., 55:
:

504. (1936) Studies on Nyctotherus ovalis, etc. Ibid., 87:10. (1947) Pelomyxa carolinensis Wilson. II. J. Morphol., 80: 93. (1951) Observations on Pelomyxa illinoisensis. Ibid., 88: 145. Kuhn, A.: (1915) Ueber Bau, Teilung und Encystierung von Bodo edax. Arch. Protist., 36:212.

Landis, E. M.: (1920) An amicronucleate race of Paramecium caudatum. Anat. Rec, 54:453. Liebmann, H.: (1944) Beitrag zur Kenntnis der Kernteilung bei vegetativen Stadien von Entamoeba coli. Arch. Protist., 97: 1. Liesche, W. (1938) Die Kern- und Fortpflanzungsverhaltnisse von Amoeba proteus. Ibid., 91:135. Lund, E. J.: (1917) Reversibility of morphogenetic processes in Bursaria. J. Exper. Zool., 24:1. Lwoff, A. (1950) Problems of morphogenesis in ciliates. New York. MacLennan, R. F.: (1937) Growth in the ciliate Ichthyophthirius. I. J. Exper. Zool, 76:243. Manwell, R. D.: (1928) Conjugation, division and encystment in
: :

Pleurotricha lanceolata. Biol. Bull., 54:417.

Mast, S. O. and Ibara, Y.: (1923) The effect of temperature, food and the age of the culture on the encystment of Didinium nasutum,. Ibid.,

45:105.

Maupas,

E.: (1888) Recherches experimentales sur la multiplication des infusoires cilies. Arch. zool. exper. (2), 6:165.

220

PROTOZOOLOGY

(1889) Le rejeunissement karyogamique chez les cilies. Ibid., 7:149. Metalnikov, S.: (1922) Dix aus de culture des infusoires sans conjugasion. C. R. Acad. Sc, 175:776. Metz, C. B.: (1946) Effects of various agents on the mating type substance of Paramecium aurelia variety 4. Anat. Rec, 93:347. (1947) Induction of "pseudo selfing" and meiosis in Paramecium aurelia by formalin killed animals of opposite mating type. J. Exp. Zool., 105:115. (1948) The nature and mode of action of the mating type substances. Am. Nat., 82:85. and Butterfield, Winifred: (1950) Extraction of a mating reaction inhibiting sgent from Paramecium calkinsi. Proc. Nat. Acad. Sc, 36:268. Mouton, H.: (1902) Recherches sur la digestion chez les amibes, etc. Ann. Inst. Pasteur, 16:457. Muller, W. (1932) Cytologische und vergleichend-physiologische Untersuchungen ueber Paramecium, etc. Arch. Protist., 78:361. Mulsow, K. (1911) Ueber Fortpflanzungserscheinungen bei Monocystis rostrata, n. sp. Ibid., 22:20. Naville, A. (1925) Recherches sur le cycle sporogonique des Aggregata. Rev. Suiss. Zool., 32:125. Noble, E. R. (1947) Cell division in Entamoeba gingivalis. Univ. California Publ. Zool., 53:263. Noland, L. E.: (1927) Conjugation in the ciliate Metopus sygmoides. J. Morphol. Physiol., 44:341. Oehler, R. (1916) Amoebenzucht auf reinem Boden. Arch. Protist., 37:175. Patten, M. W. (1921) The life history of an amicronucleate race of Didinium nasutum. Proc. Soc. Exper. Biol., 18:188. Penn, A. B. K.: (1927) Reinvestigation into the cytology of conjugation in Paramecium caudatum. Arch. Protist., 89:46. Powers, E. L.: (1943) The mating types of double animals in Euplotes patella. Am. Midland Nat., 30:175. Prandtl, H.: (1906) Die Konjugation von Didinium nasutum. Arch. Protist., 7:251. Raabe, H.: (1946) L'appareil nucleaire d'Urostyla grandis. I. Ann. Uni. Mar. Curie-Ski., Lublin, Sec. C, 1:18. (1947) II. Ibid., 1:151. Rafalko, J. S.: (1947) Cytological observations on the amoeboflagellate, Naegleria gruberi. J. Morphol., 81:1. Reichenow, E.: (1928) Ergebnisse mit der Nuclealfarbung bei Protozoen. Arch. Protist., 61:144. (1929) In: Doflein-Reichenow's Lehrbuch der Protozoenkunde. Jena. Reynolds, Mary E. C: (1932) Regeneration in an amicronucleate infusorian. J. Exper. Zool, 62:327. Rhumbler, L.: (1888) Die verschiedenen Cystenbildungen und die Entwicklungsgeschichte der holotrichen Infusoriengattung Colpoda. Zeitschr. wiss. Zool., 46:449. Rosenberg, L. E.: (1938) Cyst stages of Opisthonecta henneguyi. Tr. Am. Micr. Soc, 57:147.
:

REPRODUCTION
Schmahl, O.: (1926) Die Neubildung des Peristoms von Bursaria truncatella. Arch. Protist., 54:359.

221
bei der Teilung

Singh, B. N.: (1941) The influence of different bacterial food supplies on the rate of reproduction in Colpoda steini, etc. Ann. Appl. Biol, 27:65. (1948) Studies on giant amoeboid organisms. I. J. Gen. Microb., 2:8.

Sokoloff, B.: (1924) Das Regenerationsproblem bei Protozoen.

Arch. Protist., 47:143.

Sonneborn, T. M. (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc. Nat. Acad. Sc., 23:378. (1938) Mating types in Paramecium aurelia, etc. Proc. Am.
:

Phil.

Soc, 79:411.

(1939) Paramecium aurelia: mating types and groups, etc. Am. Nat., 73:390. (1940) The relation of macronuclear regeneration in Paramecium aurelia to macronuclear structure, etc. Anat. Rec 78:
53.

(1941) The occurrence, frequency and causes of failure to undergo reciprocal cross-fertilization, etc. Ibid., 81, Suppl.:66. (1942) Sex hormones in unicellular organisms. Cold Spr. Harb. Symp. Quant. Biol., 10:111.

(1942a) Inheritance in ciliate Protozoa. Am. Nat., 76:46. (1943) Gene and cytoplasm. I. Proc. Nat. Acad. Sc, 29: 329. (1943a) II. Ibid., 29:338. (1944) Exchange of cytoplasm at conjugation in Paramecium aurelia, variety 4. Anat. Rec, 89:49. (1947) Recent advances in the genetics of Paramecium and Euplotes. Adv. Genetics, 1:263. (1950) The cytoplasm in heredity. Heredity, 4:11. and Dippell, Ruth V.: (1943) Sexual isolation, mating types, and sexual responses to diverse conditions in variety 4, Paramecium aurelia. Biol. Bull., 85:36. (1946) Mating reactions and conjugation between varieties of Paramecium aurelia, etc. Physiol. Zool., 19:1. Sprague, V.: (1941) Studies on Gregarina blatlarum, etc., 111. Biol.

Monogr.,

18, no. 2.

Stein, F.: (1867) Der Organismus der Infusionsthiere. Pt. 2:1. Stolte, H. A.: (1922) Verlauf, Ursachen und Bedeutung der Encystierung bei Blepharisma. Verh. deutsch. zool. Gesell., 27:79. Stuart, C. A., Kidder, G. W. and Griffin, A. M.: (1939) Growth studies on ciliates. III. Physiol. Zool., 12:348. Summers, F. M.: (1935) The division and reorganization of the macronuclei of Aspidisca lynceus, etc Arch. Protist., 85: 173. (1941) The Protozoa in connection with morphogenetic problems. In: Calkins and Summers' Protozoa in biological research.

Swezy, Olive: (1922) Mitosis

coli.

in the encysted stages of Entamoeba Univ. Calif orina Publ. Zool., 20:313. Tartar, V. and Chen, T. T.: (1941) Mating reactions of enucleate fragments in Paramecium bursaria. Biol. Bull., 80:130.

222

PROTOZOOLOGY
of Col-

Taylor, C. V. and Strickland, A. G. R.: (1938) Reactions

poda duodenaria to environmental factors.
398.
I.

Arch. Protist., 90:

Thimann, K. V. and Barker, H. ment of Colpoda cucullus. II. and Haagen-Smit, A. J.:

A.: (1934) Studies on the excystExper. Zool., 69:37. (1937) Effects of salts on emergence from the cyst in Protozoa. Nature, 140:645. Thon, K.: (1905) Ueber den feineren Bau von Didinium nasutum. Arch. Protist., 5:282. Turner, J. P.: (1930) Division and conjugation in Euplotes patella, etc. Univ. California Publ. Zool., 33:193. von Brand, T. (1923) Die Encystierung bei Vorticella microstoma und hypotrichen Infusorien. Arch. Protist., 47:59. Weisz, P. B.: (1948) Time, polarity, size and nuclear content in the regneration of Stentor fragments. J. Exper. Zool., 107:269. (1950) Multiconjugation in Blepharisma. Biol. Bull., 98: 242. correlation between macronuclear thymonucleic (1950a) acid concentration and the capacity of morphogenesis in StenJ.
:

Morphol., 87:275. An experimental analysis of morphogenesis in Stentor coeruleus. J. Exper. Zool., 116:231. (1951a) A general mechanism of differentiation based on morphogenetic studies in ciliates. Am. Nat., 85:293. Wenrich, D. H.: (1939) Studies on Dientamoeba fragilis. III. J. Parasitol., 25:43. Weschenfelder, R.: (1938) Die Entwicklung von Actinocephalus parvus. Arch. Protist., 91:1. Wichterman, R. (1936) Division and conjugation in Nyctotherus J. Morphol., 60:563. cordiformis, etc.
tor. J.

(1951)

(1940) Cytogamy: a sexual process occurring in living joined pairs of Paramecium caudatum, etc. Ibid., 66:423. (1946) Further evidence of polyploidy in the conjugation of green and colorless Paramecium bursaria. Biol. Bull., 91:234. Wilson, E. B.: (1928) The cell in development and heredity. New

York.

Wolff,

E.: (1927) Un facteur de l'enkystment des amibes d'eau douce. C. R. Soc. Biol., 96:636. Woodruff, L. L.: (1921) Micronucleate and amicronucleate races of Infusoria. J. Exper. Zool., 34:329. (1931) Micronuclear variation in Paramecium bursaria. Quart. J. Micr. Sc, 74:537. (1932) Paramecium aurelia in pedigree culture for 25 years. Tr. Am. Micr. Soc, 51:196. and Erdmann, Rhoda: (1914) A normal periodic reorganization process without cell fusion in Paramecium. J. Exper. Zool., 17:425. and Spencer, H.: (1921) The survival value of conjugation in the life history of Spathidium spathula. Proc. Soc. Exper. Biol., 18:303.

Chapter

Variation and heredity

species of IS generally recognized that individuals of IT ism vary in morphological and physiological characteristics.
all

organ-

Pro-

tozoa are no exception, and manifest a wide variation in size, form, structure, and physiological characters among the members of a
single species.

The

different groups in a species are

is

spoken

of as the

races, varieties, strains, etc. It

well

known

that dinoflagellates

show a great morphological variation

in different localities.

Wesen-

berg-Lund (1908) noticed a definite seasonal morphological variation in Cerctium hirundinella in Danish lakes, while Schroder (1914) found at least nine varieties of this organism (Fig. 94) occurring in various bodies of water in Europe, and List (1913) reported that the organisms living in shallow ponds possess a marked morphological difference from those living in deep ponds. Cyphoderia ampulla is said to vary in size among those inhabiting the same deep lakes; namely, individuals from the deep water may reach 200m in length, while those from the surface layer measure only about 100^ long.
In many species of Foraminifera, the shell varies in thickness according to the part of ocean in which the organisms live. Thus the strains which live floating in surface water have a much thinner shell

than those that dwell on the bottom. For example, according to Rhumbler, Orbulina universa inhabiting surface water has a comparatively thin shell, 1.28-18^ thick, while individuals living on the bottom have a thick shell, up to 24/x in thickness. According to Uyemura, a species of Amoeba living in thermal waters, showed a
distinct dimensional difference in
different springs.
It

measured

10 40/x in diameter in sulphurous water and 45-80^ in ferrous water; in both types of water the amoebae were larger at 36-40C. than
at 51C.

diverse environmental conditions,

appear to be due to the influence of and will continue to exist under these conditions; but when the organisms of different varieties are subjected to a similar environment, the strain differences usually disappear sooner or later. That the differences in kind and amount of foods bring about extremely diverse individuals in Tetrahymena vorax and Chilomonas Paramecium in bacteria-free cultures has already been mentioned (p. 109). Chlamydomonas debaryana are repre-

Such differences or

varieties

sented by

many races differing in form,

223

localities as well as

size, and structure, in various under different laboratory conditions. Moewus

224

PROTOZOOLOGY

(1934) distinguished 12 such varieties and showed that any variety could be changed into another by using different culture media. This transformation, however, did not occur at the same rate among different races. It

was found that the longer a

strain has remained

under

Fig. 94.

Varieties of Ceratium hirundinella from various

a,

European

furcoides-type (130-300> by 30-45/x); b, brachyceroides-type (130-145/z by 30-45^); c, silesiacum-type (148-280/x by 28 34ju) d, carinthiacum-type (120-145/z by 45-60/x); e, gracile-type (140-200/* by 60-75/x); f, austriacum-type (120-160/x by 45-60/x); g, robustum-type (270-310/x by 45-55/x); h, scotticum-type (160-210/z by 50-60m); i, piburgense-type (180-260/* by 50-60/x).

waters (Schroder),
;

conditions producing a given type, the greater the time and the

ber of generations needed to change

condition, as

it

to a

new type under

numnew

is shown in Table 9. While in many species, the races or varieties have apparently been brought about into being under the influence of environmental con-

ditions, in others the inherited characters persist for a long period,

and

still

in others the biotype

may show

different inherited char-


VARIATION AND HEREDITY
Table medium and
9.

225

Relation between the

the

number of days

cultivated in peptone

number
1 to

change from type

of days cultivated in salt-sugar medium needed to type 5 in Chlamydomonas debaryana (Moewus).

Days

in

peptone medium

226

PROTOZOOLOGY

normal form

in 3 or 4 generations and that three factors appeared to determine the character and number of teeth: namely, the size of the mouth, the number and arrangement of teeth in the parent, and "something in the constitution of the clone (its genotype) which tends toward the production of a mouth of a certain size, with teeth

arrangement, and number." Races or strains have been recognized in almost all intensively studied Protozoa. For example, Ujihara (1914) and Dobell and Jepps (1918) noticed five races in Entamoeba histolytica on the basis of differences in the size of cysts. Spector (1936) distinguished two races in the trophozoite of this amoeba. The large strain was found to be pathogenic to kittens, but the small strain was not. Meleney and Frye (1933, 1935) and Frye and Meleney (1939) also hold that there is a small race in Entamoeba histolytica which has a weak capacity for invading the intestinal wall and not pathogenic to man. Sapiro, Hakansson and Louttit (1942) similarly notice two races which can
of a certain form,

be distinguished by the diameters of cysts, the division line being 10/x and 9m in living and balsam-mounted specimens respectively.

The

race with large cysts gives rise to trophozoites which are

more

actively motile, ingest erythrocytes,

and culture

easily, is

patho-

genic to

man and

kitten, while the race with small cysts develops

into less actively motile

amoebae which do not

ingest erythrocytes

and are

difficult to culture, is

not pathogenic to hosts, thus not being

however, that Cleveland and Sanders (1930) found the diameter of the cysts produced in a pureline culture of this sarcodinan, which had originated in a single cyst, varied from 7 to 23m- Furthermore, the small race of Frye and Meleney mentioned above was later found by Meleney and Zuckerman (1948) to give rise to larger forms in culture, which led the last
histozoic. It is interesting to note,

two observers to consider that the size range of the strains of this amoeba is a characteristic which may change from small to large or vice versa under different environmental conditions. Investigations by Boyd and his co-workers and others show that the species of Plasmodium appear to be composed of many strains which vary in diverse physiological characters. In an extended study on Trypanosoma lewisi, Taliaferro (1921-1926) found that this flagellate multiplies only during the first ten

days in the blood of a rat after

inoculation, after which the organisms do not reproduce. In the adult

trypanosomes, the variability for total length in a population is about 3 per cent. Inoculation of the same pure line into different rats sometimes brings about small but significant differences in the mean size

and passage through a

rat-flea generally results in a significant vari-

VARIATION AND HEREDITY

ability of the

227

pure

line. It is

considered that some differences in

dimensions
sist

among strains

are apparently due to environment (host),

but others cannot be considered as due to this cause, since they perwhen several strains showing such differences are inoculated

into the

same

host.

The two

strains of T. cruzi isolated

hosts and maintained for 28 and 41

from human months by Hauschka (1949),

showed well defined and constant

bility to the quinoline-derivative

strain-specific levels of virulence,

different degrees of affinity for certain host tissues,

unequal susceptiBayer 7602, and a difference in re-

sponse to environmental temperature. The five strains of Trichomonas gallinae studied by Stabler (1948) were found to possess a

marked variation

in virulence to its hosts.

According to Kidder and his associates, the six strains (H, E, T, T-P, W, GHH) of Tetrahymena pyriformis and the two strains (V, PP) of T. vorax differ in biochemical reactions. They found the appearance of a biochemical variation between a parent strain (T) and a daughter strain (T-P) during a few years of separation and a greater difference in the reactions between the two species than that between the strains of each species. These strains show further differences in antigenic relationships. Five strains of pyriformis contain qualitatively identical antigens, but differ quantitatively with
respect to amount, concentration or distribution of antigenic
terials.

ma-

The

sixth strain (T) contains all the antigens of the other five
strains of vorax are said to

strains

and additional antigens. The two

be nearly identical antigenically. The antigenic differences between the two species were marked, since there is no cross-reaction within
the standard testing time. In these cases, thus, some aspects of the
physiological difference

among

different strains are understood.

Paramecium caudatum to various environmental influences such as temperature and chemicals, and found that the animals develop tolerance which is inherited through many generations even after removal to the original environment. For example, one of the clones which tolerated only 1.1% of standard solution of arsenic acid, was cultivated in gradually increasing concentrations for four months, at the end of which the tolerance for this chemical was raised to 5%. After being removed to water without arsenic acid, the tolerance changed as follows: 22 days, 5%; 46 days, 4.5%; 151 days, 4%; 166 days, 3%; 183 days, 2.5%; 198 days, 1.25% and 255 days, 1%. As the organisms reproduced about once a day, the acquired increased tolerance to arsenic was inherited for about 250
Jollos (1921) subjected

generations.

There are

also

known

inherited changes in form

and structure

228

PROTOZOOLOGY

which are produced under the influence of certain environmental conditions. Jollos designated these changes long-lasting modifications (Dauermodifikationen) and maintained that a change in environmental conditions, if applied gradually, brings about a change, not in the nucleus, but in the cytoplasm, of the organism which when transferred to the original environment, is inherited for a number of generations. These modifications are lost usually during sexual processes at which time the whole organism is reorganized.

The long-lasting morphological and physiological modifications induced by chemical substances have long been known in parasitic Protozoa. Werbitzki (1910) discovered that Trypanosoma brucei loses its blepharoplast when inoculated into mice which have
been treated with pyronin, acridin, oxazin and
allied dyes,

and

Piekarski (1949) showed that trypaflavin and organic metal compounds which act as nuclear poisons and interfere with nuclear division, also bring about the loss of blepharoplast in this trypanosome. Laveran and Roudsky (1911) found that the dyes mentioned above have a special affinity for, and bring about the destruction by auto-oxidation of, the blepharoplast. Such trypanosomes lacking a blepharoplast behave normally and remain in that condition during many passages through mice. When subjected to small doses of certain drugs repeatedly, species of Trypanosoma often develop into drug-fast or drug-resistant strains which resist doses of the drug

greater than those used for the treatment of the disease for which they are responsible. These modifications may also persist for several hundred passages through host animals and invertebrate vectors,

but are eventually

lost.

Long-lasting modifications have also been produced by several investigators by subjecting Protozoa to various environmental influences during the nuclear reorganization at the time of fission,

or autogamy. In Stentor (Popoff) and Glaucoma (Chatton), long-lasting modifications appeared during asexual divisions. Calkins (1924) observed a double-type Uroleptus mobilis (Fig. 95, b) which was formed by a complete fusion of two conjugants. conjugation,
fission 367 times for 405 days, but back to normal forms, without reversion to double form. The double animal of Euplotes patella (d) is, according to Kimball (1941) and Powers (1943), said to be formed by incomplete division and rarely through conjugation. De Garis (1930) produced double animals in Paramecium caudatum through inhibition of division by exposing the animals to cyanide vapor or to low tempera-

This abnormal animal underwent

finally reverted

tures

VARIATION AND HEREDITY

229

Jennings (1941) outlined five types of long-lasting inherited changes during vegetative reproduction, as follows: (1) changes that occur in the course of normal life history, immaturity to sexual maturity which involves many generations; (2) degenerative changes resulting from existence under unfavorable conditions; (3) adaptive changes or inherited acclimitization or immunity; (4) changes which
are neither adaptive nor degenerative, occurring under specific en-

vironmental conditions; and (5) changes in form, size, and other characters, which are apparently not due to environment.

Whatever exact mechanism by which the

long-lasting modifica-

Fig. 95. a-c, Uroleptus mobilis (Calkins)

(a,

a pair in conjugation; b,

an individual from the third generation by division of a double organism which had been formed by the coalescence of a conjugating pair; c, a product of reversion); d, a double animal of Euplotes patella (Kimball).

may be, they are difficult to distinguish from permanent modification or mutation, since they persist for hundreds of generations, and cases of mutation have in most instances not been followed by sufficiently long enough pure-line cultures to definitely establish them as such (Jollos, 1934; Moewus, 1934; Sonneborn, 1947). Jollos observed that if Paramecium were subjected to environmental change during late stages of conjugation, certain individuals, if not all, become permanently changed. Possibly the recombining and reorganizing nuclear materials are affected in such a way that the hereditary constitution or genotype becomes altered. MacDougall subjected Chilodonella uncinata to ultraviolet rays and produced many changes which were placed in three groups: (1) abnormalities which caused the death of the organism; (2) temporary variations which disappeared by the third generation and (3) variations which
tions are brought about
;

230

PROTOZOOLOGY

were inherited through successive generations and hence considered as mutations. The mutants were triploid, tetraploid, and tailed diploid forms (Fig. 96), which bred true for a variable length of time in pure-line cultures, either being lost or dying off finally. The tailed form differed from the normal form in the body shape, in the number of ciliary rows and contractile vacuoles, and in the mode of movement, but during conjugation it showed the diploid number of chromosomes as in the typical form. The tailed mutant remained true and underwent 20 conjugations during ten months.

Fig.

96.

Chilodonella uncinata (MacDougall).

c, d,

view of normal individual;

a, b, ventral and side ventral and side view of the tailed mutant.

Kimball (1950) exposed Paramecium aurelia to beta particles from P 32 and obtained many clones which multiplied more slowly than normal animals or died, which conditions were interpreted by him to be due to mutational changes induced in the micronuclei by the radiation. Kimball found that the radiation was less effective if given just before the cytoplasmic division than if given at other times during the division interval and that exposure of the organisms to ultraviolet ray of wave length 2537 A inactivates
plaques containing
the

Kappa

(p. 239).

The

loss of the blepharoplast in

occurs also spontaneously in nature.

trypanosomes mentioned above A strain of Trypanosoma evansi

animals for
five years,

which had been maintained

denly

in laboratory

sud-

(Wenyon, 1928) which condition remained for 12| years (Hoare, 1940). Hoare and Bennett (1937) found five camels out of 100 they examined infected by the same species of trypanosome that was without a blepharoplast. One strain inoculost the blepharoplast

lated into laboratory animals has retained this peculiarity for nearly

VARIATION AND HEREDITY

231

three years. Nothing is known as to how such strains arise, though some workers suggest mutational change. In sexual reproduction, the nuclei of two individuals participate in producing new combinations which would naturally bring about diverse genetic constitutions. The new combination is accomplished either by sexual fusion in Sarcodina, Mastigophora, and Sporozoa, or by conjugation in Euciliata and Suctoria. The genetics of sexual fusion is only known in a few forms. Perhaps the most complete information was obtained by Moewus through his extended studies of certain Phytomonadina. In Polytoma (p. 281), Chlamydomonas (p. 276), and allied forms, the motile indi-

Two such individuals (gametes) fuse with each other and produce a diploid zygote which encysts. The zygote later undergoes at least two divisions within the cyst wall, in
viduals are usually haploid.

the

first

division of

swarmers when

by

division for

which chromosome reduction takes place. These become trophozoites and multiply asexually many generations, the descendants of each s warmer
set free

giving rise to a clone.

Moewus (1935) demonstrated the segregation and independent assortment of factors by hybridization of Polytoma. He used two varieties each of two species: P. uvella and P. pascheri, both of which possess 8 haploid chromosomes. Their constitutions were as follows:
P. uvella

Form A: Oval
(Fig. 97, a).

(F),

without papilla

(p),

with stigma

(S), large

(D)

Form B: Oval
(Fig. 97, b).

(F),

without papilla

(p),

without stigma

(s),

large (D)

P. pascheri

Form C: Pyriform
(D) (Fig. 97, c). Form D: Pyriform
(d) (Fig. 97, d).

(f),

with papilla (P), without stigma with papilla (P), without stigma

(s),

large

(f),

(s),

small

Thus

six different crosses

were possible from the four pairs of

fuse, the

characters.

When A (FpSD) and B (FpsD)

zygote divides

into four swarmers,

two lack

this cell

two swarmers have stigma (S), and the other organ, which indicates the occurrence of segrega(S, s)

tion of the

two characters
is

during the reduction division.

When

B (FpsD)
characters,

crossed with

(fPsD), thus differing in two pairs of

two swarmers possess one combination or type and the

other two another combination. Different pairs of combinations are

232
of course found. It

PROTOZOOLOGY
was found that about
(e)

half the zygotes gives rise to

b, c),

the two parental combinations (Fig. 97,

gives rise to

while the other half

FPsD

and fpsD

(/).

When B (FpsD) is crossed with D (fPsd) or A (FpSD) is crossed with D (fPsd), only two types of swarmers are also formed from each zygote, and in the case of BxD, eight different combinations are produced, while in the case of AXD, sixteen different combinations, which appear in about equal numbers, are formed. Thus these
four factors or characters
sions of the zygote.

show independent assortment during

divi-

a
Fig. 97.

b
a, b.
c, d. e, f.

Polytoma uvella. a, Form A; b, P^orm B. P. pascheri. c, Form C; d, Form D. Crosses between Forms B and C. (Moewus)

Furthermore, Moewus noticed that certain other characters appeared to be linked with some of the four characters mentioned above. For example, the length of flagella, if it is under control of a
factor,
is

linked on the

same chromosome with the

size-controlling

have invariably long flagella and small individuals short flagella. During the experiments to determine this linkage, it was found that crossing over occurs between two entire chromosomes that are undergoing synapsis. In certain races of Polytoma pascheri and Chlamydomonas eugametos, the sexual fusion takes place between members of different clones only. The zygote gives rise as was stated before to four swarmers by two divisions, which are evenly divided between the two sexes, which shows that the sex-determining factors are lodged in a single chromosome pair. In a cross between Chlamydomonas paradoxa and C. pseudoparadoxa, both of which produce only one type of gamete in a clone, the majority of the zygotes yield four clones, two
factors (D, d), for large individuals

VARIATION AND HEREDITY

small

233

producing male gametes and the other two female gametes; but a number of zygotes gives rise to four clones which contain both

gametes. It

is considered that this is due to crossing-over that brought the two sex factors (P and M) together into one chromosome, and hence the "mixed" condition, while the other chromosome which is devoid of the sex factors gives rise to individuals that soon

perish.

In crosses between Chlamydo?no?ias eugametos which possesses a stigma and 10 haploid chromosomes and C. paupera which lacks a stigma and 10 haploid chromosomes, 12 pairs of factors including sex factor are distinguishable. Consequently at least two chromosomes must have two factors in them. Thus adaptation to acid or alkaline culture media was found to be linked with differences in
the
heritance in

number of divisions in zygote. That there occurs a sex-linked inChlamydomonas was demonstrated by crossing stigma-

the opposite sex.

bearing C. eugametos of one sex with stigma-lacking C. paupera of The progeny that were of the same sex as C. euga-

metos parent possessed stigma, while those that were of the same sex as C. paupera parent lacked stigma. Thus it is seen that the sex factor
in the same chromosome. which takes place between two diploid conjugants has been studied by various investigators. Pure-line cultures of exconjugants show that conjugation brings about diverse inherited constitutions in the clones characterized by difference in

and stigma factor are located

The genetics

of conjugation

form, division-rate, mortality-rate, vigor, resistance, etc. The discovery of mating types in Paramecium and in Euplotes, and intensive studies of conjugation and related phenomena, are bringing
size,

to light hitherto

unknown information on some

of the

fundamental

problems in genetics. Sonneborn (1939) has made extended studies of variety 1 of Paramecium aurelia (p. 194) and found that genetically diverse ma-

show different types of inheritance, as follows: Stocks containing two mating types. When types I and II conjugate, among a set of exconjugants some produce all of one
terials
(1)

mating type, others all of the other mating type and still others both types (one of one type and the other of the other type). In the last mentioned exconjugants, the types segregate usually at the first division, since of the two individuals produced by the first division, one and all its progeny, are of one mating type, and the other and all its progeny are of the other mating type. A similar change was also found to take place at autogamy. Sonneborn therefore considers that the mating types are determined by macronuclei, as

234

PROTOZOOLOGY

judged by segregation at first or sometimes second division in exconjugants and by the influence of temperature during conjugation and
the
first division.

(2)

Stocks containing only one mating type.

No

conjugation ocin type

curs in such stocks.

Autogamy does not produce any change

which is always type I. Stocks that contain type II only have not yet been found. (3) Hybrids between stocks containing one and two mating types. When the members of the stock containing both types I and II (two-type condition) conjugate with those of the stock containing one type (one-type condition), all the descendants of the hybrid exconjugants show two-type condition, which shows the dominancy of two-type condition over one-type condition. The factor for the two-type condition may be designated A and that for the one-type condition a. The parent stocks are AA and aa, and all Fi hybrids Aa.

When

the hybrids (Aa) are backcrossed to recessive parent (aa)

(158 conjugating pairs in one experiment), approximately one-half

(81) of the pairs give rise to

two-type condition (Aa) and the remain-

ing one-half (77) of the pairs to one-type condition (aa), thus showing

a typical Mendelian result.

rise to

When

Fi hybrids (Aa) were interbred

by

120 conjugating pairs, each exconjugant in 88 of the pairs gave

two- type condition and each exconjugant in 32 pairs produced one-type condition, thus approximating an expected Mendelian ratio of 3 dominants to 1 recessive. That the F 2 dominants are composed of two-thirds heterozygotes (Aa) and one-third homozygotes (AA) was confirmed by the results obtained by allowing F 2 dominants to conjugate with the recessive parent stock (aa). Of 19 pairs of conjugants, 6 pairs gave rise to only dominant progenj^, which shows that they were homozygous (AA) and their progeny heterozygous (Aa), while 13 pairs produced one-half dominants and one-half recessives, which indicates that they were heterozygous (Aa) and their progeny half homozygous (aa) and half heterozygous (Aa). Thus the genie agreement between two conjugants of a pair and the relative frequency of various gene combinations as shown in these experiments confirm definitely the occurrence of meiosis and chromosomal exchange during conjugation which have hitherto been considered only on cytological ground. In Euplotes patella, Kimball (1942) made various matings with respect to the inheritance of the mating type. The results obtained can be explained if it is assumed that mating types I, II, and V, are determined by different heterozygous combinations of three allelic genes which if homozygous determine mating types III, IV, and VI.

VARIATION AND HEREDITY

Upon
and
this supposition,
is

235

type

has one

allele in

common

with type

II,

homozygous in type IV. It has one allele in common with type V, and this allele is homozygous in type VI. Type II has one allele in common with type V and this is homozygous in type mt 2 and mt 3 III. These alleles were designated by Kimball, mt The genotypes of the six mating types may be indicated as follows: imVmtMI), rn^mt 3 (II), mt 3 mt 3 (III), mtfmt (IV), mt 2 mt (V), and
this allele
1
, ,
.

mt mt 2
2

(VI).

There is no dominance among these alleles, the three heterozygous combinations determining three mating types being different from one another and from the three determined by homozygous combination. Kimball (1939, 1941) had shown that the fluid obtained free of Euplotes from a culture of one mating type will induce conjugation

among animals of certain other mating types. When all possible combinations of fluids and animals are made, it was found that the fluid from any of the heterozygous types induces conjugation among animals of any types other than its own and the fluid from any of the homozygous types induces conjugation only among animals of the types which do not have the same allele as the type from
which the fluid came. These reactions may be explained by an assumption that each of the mating type alleles is responsible for the production by the animal of a specific conjugation-inducing substance. Thus the two alleles in a heterozygote act independently of each other; each brings about the production by the animal of a substance of its own. Thus heterozygous animals are induced to conjugate only by the fluids from individuals which possess an allele
not present in the heterozygotes. The double animals of Euplotes patella (p. 228) conjugate with double animals or with single animals in appropriate mixtures and at times a double animal gives rise by binary fission to a double and

two

single animals instead of two animals (Fig. 98). Powers (1943) obtained doubles of various genotypes for mating types which were determined by observing the mating type of each of the two singles that arose from the doubles. Doubles of type IV (m^mt ) with a
1

single micronucleus (Fig. 98, a)

were mated with singles of type VI (mt 2 mt2 ) (6). The double exconjugants (d) were "split" into their component singles belonging to mating types IV and VI (g), while the doubles were type I (/) Thus it was found that the phenotype of a double animal with separate nuclei was the same as though the alleles present in the nuclei were located within one nucleus. The fact that loss of one micronucleus had no effect on the type of doubles, tends to show that the micronucleus has no direct effect on
.

236

PROTOZOOLOGY
(p.

mating types. Sonneborn's view

233) that the macro-nucleus

is

the determiner of the mating types in Paramecium aurelia appears to

hold true in Euplotes also. The relation between the cytoplasm and nucleus in respect to inheritance has become better known in recent years in some ciliates. Sonneborn (1934) crossed two clones of Paramecium aurelia differing markedly in size and division rate, and found the difference persisted

Type

VI

Type
Fig. 98.

Type

Type

Type VI

Diagram showing conjugation between a double (type IV)

and a

single (type VI) of Euplotes patella (Powers), a, a double organism with one micronucleus (genotype mt'mt1 ); b, a normal single with a mi-

cronucleus (genotype mt2 mt2 ); c, conjugation of the single with the amicronucleate half of the double (one of the pronuclei produced in the single migrates into the double, while the two pronuclei of the double undergo autogamy); d, the exconjugant double is shown to be type I (mtmit2 ); e, exconjugant single remains type VI; f, the double divides into two type I doubles; g, occasionally the anterior half of the double is widely "split," and division produces a double and two singles, the latter testing as type IV and type VI; h, line of exconjugant single. Newly formed macronuclei are stippled.

VARIATION AND HEREDITY

for a time

237

between the two Fi clones produced from the two

mem-

bers of each hybrid pair of exconjugants, but later both clones became practically identical in size and division rate (Sonneborn,
1947).

De

Garis (1935) succeeded in bringing about conjugation in

Paramecium caudatum, between the members of a large clone (198m long) (Fig. 99, a) and of a small clone (73ju long) (b). The exconjugants of a pair are different only in the cytoplasm as the nuclei are alike through exchange of a haploid set of chromosomes. The two

exconjugants divide and give rise to progeny which grow to size characteristic of each parent clone, division continuing at the rate of once or twice a day. However, as division is repeated, the descend-

0."

oooooOOOOO

Fig. 99. Diagram showing the size changes in two clones derived from a pair of conjugants of Paramecium caudatum, differing in size (a, b). Gradual change in dimensions in each clone during 22 days resulted in

intermediate size (Jennings)

ants of the large clone become gradually smaller after successive fissions, while the descendants of the small clone become gradually
larger, until at the

end of 22 days (in one experiment) both clones produced individuals of intermediate size (about 135ju long) which remained in the generations that followed. Since the exconjugants differed in the cytoplasm only, it must be considered probable that at first the cytoplasmic character was inherited through several
vegetative divisions, but ultimately the influence of the new nucleus gradually changed the cytoplasmic character. The ultimate size between the two clones is however not always midway between the
sizes of the two parent clones, and is apparently dependent upon the nuclear combinations brought about by conjugation. It has also become known that different pairs of conjugants between the same two clones give rise to diverse progeny, similar to those of

mean

sexual reproduction in Metazoa, which indicates that clones of Para-

238

PROTOZOOLOGY

mecium caudatum are in many cases heterozygous for size factors and recombination of factors occurs at the time of conjugation. In P. aurelia, Kimball (1939) observed that there occasionally occurs a change of one mating type into another following autogamy. When the change is from type II to type I, not all animals change type immediately. Following the first few divisions of the product of the first division after autogamy there are present still some type II animals, although ultimately all become transformed into type I. Here also the cytoplasmic influence persists and is inherited through
vegetative divisions. Jennings (1941) in his excellent review writes:

"The primary source of diversities in inherited characters lies in the But the nucleus by known material interchanges impresses its constitution on the cytoplasm. The cytoplasm retains the
nucleus.

constitution so impressed for a considerable length of time, dur-

and reproduces true to its impressed charremoval from contact with the nucleus to which its present constitution is due, and even for a time in the presence of another nucleus of different constitution. During this
ing which
acter. It
it

assimilates

may do this

after

period, cytoplasmic inheritance

tion.

may

occur in vegetative reproduc-

produced show the characteristics due to this cytoplasmic constitution impressed earlier by a nucleus that is no longer present. But in time the new nucleus asserts itself, impressing its own constitution on the cytoplasm. Such cycles are repeated as often as the nucleus is changed by conjugation." Since the first demonstration some forty years ago of "cytoplasmic inheritance" in higher plants, many cytoplasmic factors have been observed in various plants (Michaelis and Michaelis, 1948). Information on similar phenomena in Metazoa and Protozoa is of
cells

The new

recent origin.

As was already mentioned (p. 196), Sonneborn found in four races Paramecium aurelia a pair of characters which he designated as "killer" and "sensitive." The killers liberate paramecin, a desoxyribonucleoprotein (Wagtendonk and Zill, 1947), into
of variety 4 of

the culture
lived,

fluid, to

which they are

resistant.

When

the sensitive

races are exposed to paramecin in the fluid in which the killer race 51

hump on the oral surface toward the becomes enlarged, while the anterior part of the body gradually wastes away. The body becomes smaller and
they show after hours a
posterior end which

rounded; finally the organisms perish (Fig. 100). Sensitives can be mated to the killers, however, without injury if proper precaution is taken, since paramecin does not affect them during conjugation. The two exconjugants obtain identical genotypes, but their progeny

VARIATION AND HEREDITY

are different; that
culture.

239

one is a killer and the other is a sensitive is, obtained by selfing show no segregation. Therefore, the difference between the killer and the sensitive is due to a cytoplasmic difference and not to a genie difference. The same observer noted that the thin cytoplasmic paroral strand which appears between conjugating pair that ordinarily breaks off

F 2 progeny

within a minute, occasionally may remain for a long time, and if the strand persists as long as 30 minutes, there occurs an interchange of cytoplasm between the pair (Fig. 101). When this happens, both

exconjugants produce killer clones. In F 2 no segregation takes place. Thus killers can introduce the killer trait to sensitives through a cytoplasmic connection between them. Sonneborn supposed that the killers contain a cytoplasmic genie factor or a plasmagene which de-

Fig. 100.

Paramecium

aurelia.

The changes

leading up to death

when

the

sensitives are exposed to the killer stock 51 (variety 4) (Sonneborn).

termines the

killer trait

and
is

called

it

kappa. Preer (1948) demon-

strated that this

kappa

a particle which can be recognized in

ers

Giemsa-stained specimens (Fig. 102). It was further found that killcan be irreversibly transformed into hereditary sensitives by eliminating kappa particles by exposure to high temperature (Sonneborn, 1946), x-irradiation (Preer, 1948b) or nitrogen mustard (Geckler,

1949) and that sensitives can be transformed to hereditary killers by placing them in concentrated suspensions of broken bodies of killers (Sonneborn, 1948a). Therefore, it became clear that kappa is a self-multiplying cytoplasmic body which is produced when some are

already present.
Killer races of variety 2 differ

from each other and from that

of

variety 4 mentioned above, in the effects produced on sensitives before the latter are killed.

These sensitives possess a gene different from that of the killers and cannot be changed into killers by immersing it to kappa suspensions of broken bodies of killers. When this sensitive is mated with a killer, F 2 generation produced by self-

240
ing

PROTOZOOLOGY
among
the killer Fi clones, shows segregation of sensitives and the ratio of a single gene difference. In the presence of

killers in

dominant gene K, kappa is maintained, but in recessive k homozygotes, kappa cannot be maintained and any kappa carried over from killers is rapidly lost. Thus it is evident, Sonneborn points out, that the plasmagene kappa is dependent on gene K. Dipell (1948, 1950) found a number of killer mutants in variety 4.

End
More +h<m 3o min.

oi-

conjuqa+iorv.:

Time

until

Separated except at paroral cone. separation is completed

KHIer

Killer

Clone, clone

Killer e

Sensitive

Killer Sensitive

clone

kk+/c kk+a:
Fig. 101.
of the

KK+/C

KK+*

clone clone KK+/C KK

Diagram showing the effects of transfers of different amounts cytoplasm between mates in conjugation of kappa killers

KK+

and

KK

sensitives in

Paramecium

aurelia (Sonneborn).

She showed through breeding analysis that these mutations have brought about no change in any gene affecting kappa or the killer trait, but have been in every case due to changes in kappa. In a mutant which was capable of producing two types of killing, there were two kinds of kappa which she succeeded in separating in different animals and their progeny. Thus it became apparent that kappa can undergo mutation, that various mutant kappas can multiply in animals with the original genome, and that the kappas are determined by themselves and not by nuclear genes. According to Preer (1948), the kappa particles (Fig. 102) in the killer race G are about 0.4ju long, and those in a mutant Gml only about 0.2-0.3ju long, while in other strains they measure as much as

VARIATION AND HEREDITY

0.8/* in length.

241

Preer (1948a, 1950) further observed that the kappa

particles contain desoxyribonucleic acid

spherical), size

and number

in different races of killers,

increase, reduction or destructon of

form (rod-like or and that an the kappas, as determined by

in
of the

and vary

indirect methods,

was correlated with the observed number

Fig. 102. Photomicrographs of Paramecium, aurelia, stained with Giemsa's stain (Sonneborn). a, a killer with a number of kappa particles in the cytoplasm; b, a sensitive without kappa particles, a few darkstained bodies near the posterior end being bacteria in a food vacuole.

stained particles.

As

to the suggestion that the

etc.,

kappa

particles
is

may

be viruses, symbionts (Altenberg, 1948),

to Sonneborn (1946, 1950).

the reader

referred

The

application of antigen-antibody reactions to free-living Pro-

tozoa began some forty years ago. Bernheimer and Harrison (1940, 1941) pointed out the antigenic dissimilarity of three species of

Paramecium

in

which the members

of a clone differ widely in their

242

PROTOZOOLOGY

susceptibility to the immobilizing action of a given serum. Strains of

Tetrahymena pyriformis differ in antigenic reactions, as has already been mentioned (p. 227). Sonneborn and his co-workers have studied serological reactions in Paramecium aurelia (Sonneborn, 1950). When a rabbit is inoculated intraperitoneally with a large number

serum immobilizes in a high dilution, the organisms of the same strain, but not of other strains. Such a serologically distinct strain is called a serotype or antigenic type. It was found that a clone originating in a homozygous individual gives rise to a series of various serotypes. Race 51 gave rise to eight serotypes: A, B, C, D, E, G, H and J, and race 29, to seven serotypes:
of a strain of P. aurelia, its

H and J. When a serotype is exposed to its antiserum, changes into other types, which course Sonneborn was able to control by temperature and other conditions. For example, serotype D (stock 29) may be changed by its antiserum to type B at 32C.
A, B, C, D, F,
it

and to type H at 20C, types B, F and H are convertible one into the other and all other types can be transformed to any of the three and serotypes A and B (stock 51) are convertible one into the other, and other types can be changed to A or B. The antigenic types are inherited, if the cultures are kept at 26-27C. with food enough to
;

allow one division a day.

When

induced or spontaneous changes of

different serotypes of the
;

serotype occur, crosses

strain reveal

made among

same

gene differences among them thus all serotypes of a strain possess apparently an identical genie constitution. Sonneborn finds serotype A of stock 29 is not exactby the same as the type A of stock 51. When these are crossed, it is found that the difference between two antigens is controlled by a pair of allelic genes

no

effective

dominant over the 29A-gene. On the basis has been concluded that nuclear genes control the specificity of the physical basis of cytoplasmic inheritance in these antigenic traits, and hereditary transformations of serotype
of

which the 51A-gene

is

of these observations,

it

are cytoplasmic "mutations" of hitherto

unknown

type.

In the inheritance of the killer trait and of serotype, both traits

and inherited; hereditary changes by environmental conditions; and the traits are dependent for their maintenance upon nuclear genes. However, the specific type of killer trait is controlled by the kind of kappa present, not by the genes, while the specific type of A antigen is determined by the nuclear genes. The transformation of the killer
are cytoplasmically determined
are brought about
to the sensitive

but that of serotypes is not. mutually exclusive, as different kinds of kappa can coexist in the same organism and
is

made

irreversible,

The various types

of killer character are not

VARIATION AND HEREDITY

243

its progeny, each kind of kappa controlling production of its corresponding kind of paramecin, while in serotype, two kinds of antigen substances cannot coexist, thus being mutually exclusive. The

physical basis of the killer trait

lies in

the visible Feulgen-positive

in

kappa

particles, while

no such particles have so far been found

association with the serotype.

References

Altenburg,

E.: (1948) The role of symbionts and autocatalysts in the genetics of the ciliates. Am. Nat., 82:252. Bernheimer, A. W. and Harrison, J. A.: (1940) Antigen-antibody reactions in Paramecium: the aurelia group. J. Immunol.,

39:73.
(1941) Antigenic
differentiation

among

strains
:

of

Paramecium
:

aurelia. Ibid., 41:201.

Calkins, G. N. (1925) Uroleptus mobilis. V. J. Exper. Zool., 41 191. Cleveland, L. R. and Sanders, Elizabeth P.: (1930) Encystation, multiple fission without encystment, etc. Arch. Protist., 70:
223.

Garis, C. F.: (1930) Genetic results from conjugation of double monsters and free individuals of Paramecium caudatum. Anat. Rec, 47:393. (1930a) Nucleus versus cytoplasm in the heredity of Paramecium caudatum as shown by conjugation of double monsters. Ibid., 47:393. (1935) Heritable effects of conjugation between free individuals and double monsters in diverse races of Paramecium. J. Exper. Zool., 71:209. Dippell, Ruth V.: (1948) Mutation of the killer plasmagene, Kappa, in variety 4 of Paramecium aurelia. Am. Nat., 82:43. (1950) Mutation of the killer cytoplasmic factor in Paramecium aurelia. Heredity, 4:165. Dobell, C. and Jepps, Margaret W.: (1918) A study of the diverse races of Entamoeba histolytica distinguishable from one another by the dimensions of their cysts. Parasitology, 10:320. Frye, W. W. and Meleney, H. E.: (1938) The pathogenicity of a strain of small race Entamoeba histolytica. Am. J. Hyg., 27:580. Furgason, W. H.: (1940) The significant cytostomal pattern of the "Glaucoma-Colpidium group," and a proposed new genus and species, Tetrahymena geleii. Arch. Protist., 94:224. Geckler, R, P.: (1949) Nitrogen mustard inactivation of the cytoplasmic factor, kappa, in Paramecium. Science, 110:89. Hauschka, T. S.: (1949) Persistence of strain-specific behavior in two strains of Trypanosoma cruzi after prolonged transfer through inbred mice. J. Parasit., 35:593. Hegner, R. W. (1919) Heredity, variation, and the appearance of diversities during the vegetative reproduction of Arcella dentata.
:

De

Genetics, 4:95.

244

PROTOZOOLOGY
C. A.: (1940) Recent studies on the kinetoplast in relation to heritable variation in trypanosomes. J. Roy. Micr. Soc., 60:
2G.

Hoare,

(1943) Biological races in parasitic Protozoa. Biol. Rev., 18:

137.

and Bennett,
studies on

S. C. J.: (1937)

Morphological and taxonomic

III. Parasitology. 29:43. (1939) IV. Ibid., 30:529. Jennings, H. S.: (1909) Heredity and variation in the simplest organisms. Am. Nat., 43:322. (1916) Heredity, variation and the results of selection in the uniparental reproduction of Difflugia corona. Genetics, 1 :407. (1929) Genetics of the Protozoa. Bibliogr. Genetica, 5:105. (1937) Formation, inheritance and variation of the teeth in Difflugia corona. J. Exper. Zool., 77:287. (1938) Sex reaction types and their interrelations in Paramecium bursaria. I. Proc. Nat. Acad. Sc, 24:112. (1939) Genetics of Paramecium bursaria. I. Genetics, 24:202. (1941) Inheritance in Protozoa. In: Calkins and Summers' (1941) Protozoa in biological research. New York. Raffel, D., Lynch, R. S. and Sonneborn, T. M.: (1932) The diverse biotypes produced by conjugation within a clone of
,

mammalian trypanosomes.

Paramecium. J. Exper. Zool., 63:363. Jollos, V.: (1913) Experimentelle Untersuchungen an Infusorien. Biol. Zentralbl., 33:222. (1921) Experimentelle Protistenstudien. I. Arch. Protist.,
43:1. (1934) Dauermodifikationen und Mutationen bei Protozoen. Ibid., 83: 197. Kidder, G. W., Stuart, C. A., McGann, Virginia G. and Dewey, Virginia C.: (1945) Antigenic relationships in the genus Tetrahymena. Physiol. Zool., 18:415. Kimball, R. F.: (1939) delayed change of phenotype following a change of genotype in Paramecium aurelia. Genetics, 24:49. - (1939a) Mating types in Euplotes. Am. Nat., 73:451. (1941) Double animals and amicronucleate animals in Euplotes patella with particular reference to their conjugation. J. Exper. Zool., 86:1. (1942) The nature and inheritance of mating types in Euplotes patella. Genetics, 27:269. (1950) The effect of radiations on genetic mechanism of

List,

aurelia. J. Cell. Comp. Physiol., 35 (sup. 1) 157. (1913) Ueber die Temperal- und Lokalvariation von Ceratium hirundinella, etc. Arch. Hydrobiol., 9:81. Meleney, H. E. and Zuckerman, Lucille K.: (1948) Note on a strain of small race Entamoeba histolytica which became large

Paramecium
T.:

in culture.

Am.

J.

Hyg., 47:187.

Michaelis, P. and Michaelis, G.: (1948) Ueber die Konstanz des zytoplasmons bei Epilobium. Planta, 35:467.

VARIATION AND HEREDITY

Moewus,

245

F.: (1933) Untersuchungen ueber die Variabilitat von Chlamydomonaden. Arch. Protist., 80:128. (1934) Ueber Dauermodifikation bei Chlamydomonaden.
Ibid., 83:220.

(1935) Ueber die Vererbung des Geschlechts bei Polytoma pascheri und bei P. uvella. Ztschr. Induk. Abst.-u. Vererb., 69: 374. (1936) Faktorenaustausch, insbesondere der Realisatoren bei Chlamydomonas-Kreuzungen. Ber. deutsch. Bot. Ges., 54:
45.

(1938) Vererbung des Geschlechts bei Chlamydomonas eugametos und verwandten Arten. Biol. Zentralbl., 58:516. Piekarski, G.: (1949) Blepharoplast und Trypaflavinwirkung bei Trypanosoma brucei. Zentralbl. Bakt., I. Orig., 153:109. Powers, E. L.: (1943) The mating types of double animals in Euplotes patella. Am. Midi. Natur., 30:175. Preer, J. R. Jr.: (1948) The killer cytoplasmic factor kappa: its rate of reproduction, the number of particles per cell, and its size. Am. Nat., 82:35. (1948a) Microscopic bodies in the cytoplasm of "killers" of Paramecium aurelia and evidence for the identification of these bodies with cytoplasmic factor, kappa. Genetics, 33:625. (1950) Microscopically visible bodies in the cytoplasm of the "killer" strain of Paramecium aurelia. Ibid., 35:344. Reynolds, B. D. (1924) Interactions of protoplasmic masses in relation to the study of heredity and environment in Arcella polypora. Biol. Bull., 46:106. Root, F. M.: (1918) Inheritance in the asexual reproduction in Centropyxis aculeata. Genetics, 3:173. Sapiro, J. J., Hakansson, E. G. and Louttit, C. M.: (1942) The occurrence of two significantly distinct races of Entamoeba histolytica. Am. J. Trop. Med., 22:191. Schroder, B.: (1914) Ueber Planktonepibionten. Biol. Zentralbl., 34:328. Sonneborn, T. M. (1937) Sex, sex inheritance and sex determination in Paramecium aurelia. Proc. Nat. Acad. Sc, 23:378. (1939) Paramecium aurelia: mating types and groups; etc. Am. Nat., 73:390. (1942) Inheritance in ciliate Protozoa. Ibid., 76:46. (1943) Gene and cytoplasm. I, II. Proc. Nat. Acad. Sc, 29:
:
:

329. (1946) Experimental control of the concentration of cytoplasmic genetic factors in Paramecium. Cold Springs Harbor
Biol., 11:236. (1947) Recent advances in the genetics of Paramecium and Euplotes. Adv. Genetics, 1:263. (1948) Introduction to symposium on plasmagenes, genes and characters in Paramecium aurelia. Am. Nat., 82:26. (1950) The cytoplasm in heredity. Heredity, 4:11.

Symp. Quant.

246

PROTOZOOLOGY
and Lynch, R. S.: (1934) Hybridization and segregation Paramecium aurelia. J. Exper. Zool., 67:1.
in

Stabler, R. M.: (1948) Variations in virulenec of strains chomonas gallinae in pigeons. J. Parasit., 34: 147. Taliaferro, W. H.: (1926) Variability and inheritance of Trypanosoma lewisi. J. Exper. Zool., 43:429.

of Trisize in

(1929) The immunology of parasitic infections. New York. and Huff, C. G.: (1940) The genetics of the parasitic Protozoa. Am. A. Adv. Sc. Publ., 12:57. Ujihara, K.: (1914) Studien ueber die Amoebendysenterie. Ztschr.

Hyg., 77:329.
J. v. and Zill, L. P.: (1947) Inactivation of ("killer" substance of Paramecium aurelia 51, variety 4) at different hydrogen-ion concentrations and temperatures. J. Biol. Chem., 171:595. Wenyon, C. M. (1928) The loss of the parabasal body in trypano-

Wagtendonk, W.
paramecin

somes. Tr. Roy. Soc. Trop. Med. Hyg., 22:85.

Wesenberg-Lund,
lakes.

C.

(1908) Plankton investigations of the Danish

Copenhagen.

PART

II:

TAXONOMY AND

SPECIAL BIOLOGY

Chapter

Major groups and phylogeny

Protozoa grouped THE 254) and Ciliophora
are
tive Protozoa
(p. 254),

of Protozoa

into

(p. 683).

two subphyla: Plasmodroma (p. The Plasmodroma are more primi-

and subdivided into three classes: Mastigophora (p. 417), and Sporozoa (p. 526). The Ciliophora possess more complex body organizations, and are divided into two classes: Ciliata (p. 683) and Suctoria (p. 863). In classifying Protozoa, the natural system would be one which is based upon the phylogenetic relationships among them in conformity with the doctrine that the present day organisms have descended from primitive ancestral forms through organic evolution. Unlike Metazoa, the great majority of Protozoa now existing do not possess skeletal structures, which condition also seemingly prevailed among their ancestors, and when they die, they disintegrate and leave nothing behind. The exceptions are Foraminifera (p. 493) and Radiolaria (p. 516) which produce multiform varieties of skeletal structures composed of inorganic substances and which are found abundantly preserved as fossils in the earliest fossiliferous strata. These fossils show clearly that the two classes of Sarcodina were
Sarcodina
already well-differentiated groups at the time of fossilization.

The

sole information the palaeontological record reveals for our reference

is

that the differentiation of the major groups of Protozoa must have

consideration of phylogeny of Protozoa had to depend ex-

occurred in an extremely remote period of the earth history. Therefore,

upon the data obtained through morphological, physioand developmental observations of the present-day forms. The older concept which found its advocates until the beginning of the present century, holds that the Sarcodina are the most primitive of Protozoa. It was supposed that at the very beginning of the living world, there came into being undifferentiated mass of protoplasm which later became differentiated into the nucleus and the cytoplasm. The Sarcodina represented by amoebae and allied forms do not have any further differentiation and lack a definite body wall, they are, therefore, able to change body form by forming pseudopodia. These pseudopodia are temporary cytoplasmic processes and formed or withdrawn freely, even in the more or less permanent axopodia. On the other hand, flagella and cilia are permanent cell-organs possessing definite structural plans. Thus from
clusively
logical,

the morphological viewpoint, the advocates of this concept main-

249

250

PROTOZOOLOGY
and which gave
rise to

tained that the Sarcodina are the Protozoa which were most closely
related to ancestral forms
Ciliata,

Mastigophora,
does not agree

and Sporozoa. This concept is however

difficult to follow, since it

with the general belief that the plant came into existence before the animal; namely, holophytic organisms living on inorganic substances anteceded holozoic organisms living on organic substances. There-

from the physiological standpoint the Mastigophora which number of chlorophyll-bearing forms, must be considered as more primitive than the holozoic Sarcodina. The class Mastigophora is composed of Phytomastigina (chromatophore-bearing flagellates and closely related colorless forms) and Zoomastigina (colorless flagellates). Of the former, Chrysomonadina (p. 256) are mostly naked, and are characterized by possession of 1-2 flagella, 1-2 yellow chromatophores and leucosin. Though holophytic nutrition is general, many are also able to carry on holozoic nutrition. Numerous chrysomonads produce pseudopodia of different types; some possess both flagellum and pseudopodia; others such as Chrysamoeba (Fig. 105) may show flagellate and ameoboid forms (Klebs;
fore,

include a vast

Scherffel);
(p. 267),

still

others, for example,

members

of

Rhizochrysidina

may

lack flagella completely, though retaining the char-

acteristics of
(p.

Chrysomonadina.

When

individuals of Rhizochrysis

267) divide, Scherffel (1901) noticed unequal distribution of the chromatophore resulted in the formation of colorless and colored
a, b). Pascher (1917) also observed that in the chrysomonad, Chrysarachnion (p. 267), the division of component individuals produces many in which the chromatophore is entirely lacking (Fig. 110, c, d). Thus these chrysomonads which lack chromatophores, resemble Sarcodina rather than the parent Chryosomonadina. Throughout all groups of Phytomastigina, there occur forms which are morphologically alike except the presence or absence of chromatophores. For example, Cryptomonas (p. 273) and Chilomonas (p. 273), the two genera of Cryptomonadina, are so morphologically alike that had it not been for the chromatophore, the former can hardly be distinguished from the latter. Other examples are Euglena, Astasia, and Khawkinea; Chlorogonium and Hyalogonium; Chlamydomonas and Polytoma; etc. The chromatophores of various Phytomastigina degenerate readily under experimental conditions. For instance, Zumstein (1900) and recently Pringsheim and Hovasse (1948) showed that Euglena gracilis loses its green coloration even in light if cultured in fluids

individuals (Fig. 110,

colonial

MAJOR GROUPS AND PHYLOGENY

rich in organic substances; in a culture fluid with a small
of organic substances, the
it

251

amount

in darkness;

the flagellates in darkness. Therefore, it would appear reasonable to consider that the morphologically similar forms with or without chromatophores such as are cited above, are closely related to each other phylogenetically, that they should be grouped together in any scheme of classification, and that the apparent heterogeneity among Phytomastigina is due to the natural course of events. The newer concept which is at present followed widely is that the Mastigophora are the most primitive unicellular animal organisms.

and when cultured remain green even

organisms retain green color in light, lose in a pure inorganic culture fluid,

Of Mastigophora, Phytomastigina are to be considered on the same ground more primitive than Zoomastigina. According to the studies of Pascher, Scherffel and others, Chrysomonadina appear to be the nearest to ancestral forms from which other groups of Phyto-

Among Zoomastigina, Rhizomastigina possibly Protomonadina, from which Polymastigina and Hypermastigina later arose. The last-mentioned group is the most highly advanced one of Mastigophora in which an increased number of flagella is an outstanding characteristic. As to the origin of Sarcodina, many arose undoubtedly from various Zoomastigina, but there are indications that they may have evolved directly from Phytomastigina. As was stated already, Rhizochrysidina possess no flagella and the chromatophore often degenerates or is lost through unequal distribution during division, apparently being able to nourish themselves by methods other than holophytic nutrition. Such forms may have given rise to Amoebina. Some chrysomonads such as Cyrtophora (p. 260) and Palatinella, have axopodia, and it may be considered that they are closer to the ancestral forms from which Heliozoa arose through stages such as shown by Actinomonas (p. 335), Dimorpha (p. 335), and Pteridomonas (p. 335) than any other forms. Another chrysomonad, Porochrysis (p. 260), possesses a striking resemblance to Testacea. The interesting marine chrysomonad, Chrysothylakion (p. 267) that produces a brownish calcareous test from which extrudes anastomosing rhizopodial network, resembling a monothalamous foraminiferan, and forms such as Distephanus (p. 267) with siliceous skeletons, may depict the ancestral forms of Foraminifera and Radiolaria respectively. The flagellate origin of these two groups of Sarcodina is also seen in the appearance of flagellated swarmers during their development. The Mycetozoa show also flagellated phase
mastigina arose.
rise to

gave

252

PROTOZOOLOGY
life

which perhaps suggests their origin in flagelchrysomonad Myxochrysis (p. 261), Pascher (1917) finds a multinucleate and chromatophore-bearing organism (Fig. 105, e-j) that stands intermediate between Chrysomonadina and Mycetozoa. Thus there are a number of morphological, developmental, and physiological observations which sugduring their
cycle,

lated organisms. In fact, in the

gest the flagellate origin of various Sarcodina.

The Sporozoa appear to be equally

polyphyletic.

The Telosporidia

contain three groups in which flagellated microgametes occur, which suggests their derivation from flagellated organisms. Leger and

Duboscq even considered them

to have arisen from

Bodonidae

(p.

362) on the basis of flagellar arrangement. Obviously Gregarinida are the most primitive of the three groups. The occurrence of such a

form as Selenococcidium (p. 572), would indicate the gregarineorigin of the Coccidia and the members of Haemogregarinidae (p. 592) suggest the probable origin of the Haemosporidia in the Coc-

The Cnidosporidia are characterized by multinucleate troby the spore in which at least one polar capsule with a coiled filament occurs. Some consider them as having evolved
cidia.

phozoites and

from Mycetozoa-like organisms, because of the similarity in multinucleate trophozoites, while others compare the polar filament with
the flagellum. It
is

interesting to note here that the nematocyst,

similar to the polar capsule, occurs in certain Dinoflagellata (p. 310)

independent of flagella. The life cycle of Acnidosporidia is still incompletely known, but the group may have differentiated from such Sarcodina as Mycetozoa. The Ciliata and Suctoria are distinctly separated from the other groups. They possess the most complex body organization seen among Protozoa. All ciliates possess cilia or cirri which differ from flagella essentially only in size. Apparently Protociliata and Euciliata have different origins, as judged by their morphological and physiological differences. It is probable that Protociliata arose from forms which gave rise to Hypermastigina. Among Euciliata, one finds such forms as Coleps, Urotricha, Plagiocampa, Microregma, Trimyema, Anophrys, etc., which have, in addition to numerous cilia, a long flagellum-like process at the posterior end, and Ileonema that possesses an anterior vibratile flagellum and numerous cilia, which also indicates flagellated organisms as their ancestors. It is reasonable to assume that Holotricha are the most primitive ciliates from which Spirotricha, Chonotricha, and Peritricha evolved. The Suctoria are obviously very closely related to Ciliata and most probably arose from ciliated ancestors by loss of cilia during adult stage

MAJOR GROUPS AND PHYLOGENY

253

and by developing tentacles in some forms from cytostomes as was suggested by Collin (Fig. 13). General reference (Franz, 1919; Lwoff,
1951).

References

Butschli, 0.: (1883-1887) Bronn's Klassen und Ordnungen des

Thierreichs.
1.

Doflein, F. and E. Reichenow: (1949) Lehrbuch der Protozoenkunde. 6th ed.

1.

Franz, V.: (1919) Zur Frage der phylogenetischen Stellung der

Protisten, besonders der Protozoen. Arch. Protist., 39:263.

Lwoff, A.: (1951) Biochemistry and physiology

York.

of Protozoa.

New

Minchin, E. A.: (1912) Introduction to the study of the Protozoa. London. Pascher, A.: (1912) Ueber Rhizopoden- und Palmellastadien bei
Flagellaten, etc. Arch. Protist., 25:153. (1916) Rhizopodialnetz als Fangvorrichtung bei einer Plas-

modialen Chrysomonade. Ibid., 37:15. (1916a) Fusionsplasmodien bei Flagellaten und ihre Bedeutung fiir die Ableitung der Rhizopoden von den Flagellaten.
Ibid., 37:31.

(1917) Flagellaten

und Rhizopoden

in ihren gegenseitigen

Beziehungen. Ibid., 38:1.

(1942) Zur Klarung einiger gefarbter und farbloser Flagellaten und ihrer Einrichtungen zur Aufnahme animalischer Nahrung. Ibid., 96:75. Pringsheim, E. G. and Hovasse, R.: (1948) The loss of chromatophores in Euglena gracilis. New Phytologist, 47:52. Scherffel, A.: (1901) Kleiner Beitrag zur Phylogenie einiger Gruppen niederer Organismen. Bot. Zeit., 59:143. Zumstein, H.: (1900) Zur Morphologie und Physiologie der Euglena gracilis. Jahrb. wiss. Botanik., 34:149.

Chapter

Phylum Protozoa Goldfuss

Subphylum
1

Plasmodroma Doflein

Plasmodroma possess pseudopodia which are used for locomotion and food-getting or flagella that serve for cell-organs of locomotion. In Sporozoa, the adult stage does not possess any cellorgans of locomotion. The body structure is less complicated than that of Ciliophora. In some groups, are found various endo- and exo-skeletons. The nucleus is of one kind, but may vary in number. All types of nutrition occur. Sexual reproduction is exclusively by sexual fusion or automixis; asexual reproduction is by binary or multiple fission or budding. The majority are free-living, but numerous parasitic forms occur, Sporozoa being
all parasitic.

THE

The Plasmodroma

are subdivided into three classes as follows:

Trophozoite with fiagellum Class 1 Mastigophora Trophozoite with pseudopodium Class 2 Sarcodina (p. 417) Without cell-organs of locomotion; producing spores; all parasitic Class 3 Sporozoa (p. 526)

Class

Mastigophora Diesing

The

Mastigophora includes those Protozoa which possess one to

several flagella. Aside from this

common

characteristic, this class

makes a very heterogeneous assemblage and seems to prevent a sharp distinction between the Protozoa and the Protophyta, as it includes Phytomastigina which are often dealt with by botanists.
In the majority of Mastigophora, each individual possesses 1-4 during the vegetative stage, although species of Polymastigina may possess up to 8 or more flagella and of Hypermastigina a greater number of flagella. The palmella stage (Fig. 103) is common among the Phytomastigina and the organism is capable in this stage not only of metabolic activity and growth, but also of reproduction. In this respect, this group shows also a close relationship to algae. All three types of nutrition, carried on separately or in combination, are to be found among the members of Mastigophora. In holophytic forms, the chlorophyll is contained in the chromatophores which are of various forms among different species and which differ in colors, from green to red. The difference in color appears to be due to the pigments which envelop the chlorophyll body (p. 89). Many forms adapt their mode of nutrition to changed environmental conditions; for instance, from holophytic to saprozoic in the absence of the sunlight. Holozoic, saprozoic and holophytic nutrition are said
flagella

254

MASTIGOPHORA
to be

255

combined in such a form as Ochromonas. In association with chromatophores, there occurs refractile granules or bodies, the pyrenoids, which are connected with starch -form at ion. Reserve

food substances are starch, oil, etc. (p. 113). In less complicated forms, the body is naked except for a slight cortical differentiation of the ectoplasm to delimit the body surface

and

is

plastic pellicle

capable of forming pseudopodia. In others, there occurs a thin produced by the cytoplasm, which covers the body
still

surface closely. In

others, the

cased in a

shell, test, or lorica,

which

body form is constant, being enis composed of chitin, pseudogelatinous secretion envelops
is

chitin, or cellulose.

Not infrequently a

the body. In three families of Protomonadina there

protrudes.

a collar-like

structure located at the anterior end, through which the flagellum

The great majority of Mastigophora possess a single nucleus, and only a few are multinucleated. The nucleus is vesicular and contains a conspicuous endosome. Contractile vacuoles are always present in
the forms inhabiting fresh water. In simple forms, the contents of the vacuoles are discharged directly through the body surface to
the exterior; in others there occurs a single contractile vacuole near a reservoir which opens to the exterior through the so-called cyto-

pharynx. In the Dinoflagellata, there are apparently no contractile vacuoles, but non-contractile pusules (p. 310) occur in some forms. In chromatophore-bearing forms, there occurs usually a stigma which is located near the base of the flagellum and seems to be the center of phototactic activity of the organism which possesses it. Asexual reproduction is, as a rule, by longitudinal fission, but in some forms multiple fission also takes place under certain circumstances, and in others budding may take place. Colony-formation
(p.

174),

due to incomplete separation

of

daughter individuals,

is

widely found

among this group. Sexual reproduction has been reported in a number of species. The Mastigophora are free-living or parasitic. The free-living forms are found in fresh and salt waters of every description many
;

submerged objects, and still others are sessile. Together with algae, the Mastigophora compose a major portion of plankton life which makes the
are free-swimming, others creep over the surface of

foundation for the existence of all higher aquatic organisms. The parasitic forms are ecto- or endo-parasitic, and the latter inhabit either the digestive tract or the circulatory system of the host animal. Trypanosoma, a representative genus of the latter group, includes important disease-causing parasites of man and of domestic
animals.

256

PROTOZOOLOGY
into

The Mastigophora are divided

With chromatophores Without chromatophores
Subclass
1

two subclasses

as follows

Subclass 1 Phytomastigina Subclass 2 Zoomastigina (p. 333)

Phytomastigina Doflein

The Phytomastigina possess the chromatophores and their usual method of nutrition is holophytic, though some are holozoic, saprozoic or mixotrophic; the majority are conspicuously colored; some
that lack chromatophores are included in this group, since their
structure and development resemble closely those of typical Phyto-

mastigina.

Some

observers consider the types of flagella as one of the char-

acters in taxonomic consideration (Petersen, 1929; Vlk, 1938:

Owen,

1949; etc.).

Owen found,

for example, "lash flagella" (with a terminal

filament) in some species of Phytomonadina, Rhizomastigina, Protomonadina and Polymastigina and simple flagella in the forms included in Chrysomonadina, Cryptomonadina, Euglenoidina and Dinoflagellata; and simple flagellum and flagella on Oikomonas and Monas. He advocated the transfer of the latter two genera from Protomonadina to Chrysomonadina.
1-4 flagella, either directed anteriorly or trailing Chromatophores yellow, brown or orange Order 1 Chrysomonadina Anabolic products fat, leucosin Anabolic products starch or similar carbohydrates Order 2 Cryptomonadina (p. 272) Chromatophores green Anabolic products starch and oil. Order 3 Phytomonadina (p. 276) Anabolic products paramylon Order 4 Euglenoidina (p. 293) Anabolic products oil Order 5 Chloromonadina (p. 306) Order 6 Dinoflagellata (p. 310) 2 flagella, one of which transverse

Order

Chrysomonadina Stein
and are
plastic, since

The chrysomonads
brown and usually

are minute organisms

the majority lack a definite cell- wall. Chromatophores are yellow to

discoid, though sometimes reticulated, in form. Metabolic products are leucosin and fats. 1-2 flagella are inserted at or near the anterior end of body where a stigma is present. Many chrysomonads are able to form pseudopodia for obtaining food materials which vary among different species. Nutrition, though
chiefly holophytic,
is

also holozoic or saprozoic. Contractile vacuoles

are invariably found in freshwater forms,

and are ordinarily

chrysomonads

of

simple structure.

Under conditions not

fully understood, the

lose

MASTIGOPHORA, CHRYSOMONADINA

257

their fiagella and undergo division with development of mucilaginous envelope and thus transform themselves often into large bodies known as the palmella phase and undertake metabolic activities as well as multiplication (Fig. 103). Asexual reproduction is, as a rule,

w
Qb
b

m
Fig. 103.

The

life-cycle of

Chromulina,

X about
d,

ment;

b, fission; c,

colony-formation;

200 (Kiihn). a, encystpalmella-formation.

division during either the motile or the palmella Incomplete separation of the daughter individuals followed by repeated fission, results in numerous colonial forms mentioned elsewhere (p. 174). Some resemble higher algae very closely. Sexual
stage.

by longitudinal

Encystment occurs comis unknown in this group. monly; the cyst is often enveloped by a silicious wall possessing an opening with a plug. Taxonomy (Doflein, 1923; Schiller, 1925a; Pascher, 1926; Conrad, 1926; Scherffel, 1926; Hollande, 1952). The chrysomonads inhabit both fresh and salt waters, often occurring abundantly in plankton.
reproduction
Motile stage dominant Palmella stage dominant
Sarcodina-like; flagellate stage

Suborder

Euchrysomonadina

unknown
Suborder 2 Rhizochrysidina Suborder 3 Chrysocapsina
(p.

With

flagellate

phase
1

(p.

267) 269)

Suborder
With or without simple One flagellum

Euchrysomonadina Pascher
Family
1

shell

Chromulinidae

(p.

258)

2 flagella Family 2 Syncryptidae Fiagella equally long Family 3 Ochromonadidae Flagella unequally long With calcareous or silicious shell .Family 4 Coccolithidae Bearing calcareous discs and rods. Family 5 Silicoflagellidae Bearing silicious skeleton
. .

(p. (p.

262) 264)
266) 267)

(p. (p.

258

PROTOZOOLOGY
Family
1

Chromulinidae Engler

shell; with a single flagellum; often with rhizopodia; a few colonial; free-swimming or at-

Minute forms, naked or with sculptured

tached.

Genus Chromulina Cienkowski. Oval; round in cross-section; amoeboid; 1-2 chromatophores palmella stage often large; in fresh water. Numerous species. The presence of a large number of these organisms gives a golden-brown color to the surface of the water.
;

Development
C. pascheri

(Doflein, 1923); species (Doflein, 1921, 1922; Schiller,

1929; Pascher, 1929; Conrad, 1930).

Hofeneder

(Fig. 104, a, b). 15-20/* in diameter.

Genus Pseudochromulina Doflein. Spheroid body amoeboid; cytoplasm granulated; two contractile vacuoles anterior; a single flagellum about the body length; a yellow tray-like chromatophore with upturned edge; stigma and pyrenoid absent; nucleus central; cyst
ovoid, with asymmetrical siliceous wall with an aperture tube (Doflein,

1921).

P. asymmetrica D.

Body 3-4
4/*

/*

in

diameter; cytoplasm with fat and

aperture tube about
l/i;

probably leucosin; cyst water (Doflein, 1921).

by

3/*;

fresh

Genus Chrysamoeba Klebs. Body naked;

flagellate stage ovoid,

with 2 chromatophores, sometimes slender pseudopodia at the same time; flagellum may be lost and the organism becomes amoeboid, resembling Rhizochrysis (p. 267) standing fresh water.
;

K. (Fig. 105, a, b). Flagellated form measures 8/x by 3.5/*; amoeboid stage about 8-10/* by 3-4/x, with 10-20/x long radiating pseudopodia; cyst 7/* in diameter (Doflein, 1922). Genus Chrysapsis Pascher. Solitary; plastic or rigid; chromatophore diffused or branching; with stigma; amoeboid movement;
C. radians

holophytic, holozoic; fresh water. Several species.

C. sageneF. (Fig. 104,
c).

Anterior region actively plastic; stigma

small; 8-14m long; flagellum about 30/* long.

Genus Chrysococcus Klebs. Shell spheroidal or ovoidal, smooth and often brown-colored; through an opening a flagellum protrudes; 1-2 chromatophores; one of the daughter individuals formed by binary fission leaves the parent shell and forms a new one fresh water. Lackey (1938) found several species in Scioto River,
or sculptured

Ohio.

by 7-10/*. Genus Mallomonas Perty (Pseudomallomonas Chodat). Body elongated; with silicious scales and often spines; 2 chromatophores
C. ornatus Pascher (Fig. 104, d). 14-16/*

MASTIGOPHORA, CHRYSOMONADINA
rod-shaped; fresh water.
1927, 1930).

259

Numerous
e).

species (Pascher, 1921; Conrad,

litomosa Stokes (Fig. 104,

Scales very delicate, needle-like

projections at both ends; flagellum as long as body; 24-32/*

by

8/x-

sagene,

Fig. 104. a, b, Chromulina pascheri, X670 (Hofeneder); c, Chrysapsis X1000 (Pascher); d, Chrysococcus ornatus, X600 (Pascher); e, Mallomonas litomosa, X400 (Stokes); f, Pyramidochrysis modesta, X670 (Pascher); g, Sphaleromantis ochracea, X600 (Pascher); h, Kephyrion ovum, X1600 (Pascher); i, Chrysopyzis cyathus, X600 (Pascher); j, Cyrtophora pedicellata, X400 (Pascher); k, Palatinella cyrtophora, X400 (Lauterborn) 1, Chrysosphaerella longispina, X600 (Lauterborn).
;

260

PROTOZOOLOGY

firm envelope in the surface of which are

Genus Microglena Ehrenberg. Body ovoid to cylindrical; with a embedded many lenticular
silica

masses of
reservoir

(Conrad, 1928); a single flagellum at anterior end; a

around which four to eight contractile vacuoles occur; a sheet-like chromatophore; stigma; leucosin; fresh water. M. ovum Conrad (Fig. 106, a). 31-38ju by 18-25m (Conrad, 1928). Genus Pyramidochrysis Pascher. Body form constant; pyriform with 3 longitudinal ridges; flagellate end drawn out; a single chromatophore; 2 contractile vacuoles; fresh water.
P. modesta P. (Fig. 104,/). 11-13/z long.

Genus Sphaleromantis Pascher. Triangular

vacuoles stigma large; long flagellum; fresh water.
;

or

heart-shaped;

highly flattened; slightly plastic; 2 chromatophores; 2 contractile

S. ochracea P. (Fig. 104, g).

6-13m long.
or fusiform lorica
;

Genus Kephyrion Pascher. With oval

body

fills

posterior half of lorica; one chromatophore; a single short flagellum;

small; fresh water. Species (Conrad, 1930).

K. ovum P. (Fig. 104, h). Lorica up to 7 p. by 4;u. Genus Chrysopyxis Stein. With lorica of various forms, more
less flattened;

or

1-2 chromatophores; a flagellum; attached to algae in

i).

fresh water.
C. cyathus Pascher (Fig. 104,

One chromatophore;

flagellum

twice body length; lorica 20-25^

by

12-15/x.

Genus Cyrtophora Pascher. Body inverted pyramid with 6-8 axopodia and a single flagellum; with a contractile stalk; a single chromatophore a contractile vacuole fresh water. C. pedicellata P. (Fig. 104, j). Body 18-22julong; axopodia 40-60m
;
;

long; stalk 50-80;u long.

Genus Palatinella Lauterborn. Lorica tubular; body heartshaped

anterior border with 16-20 axopodia; a single flagellum; a chromato-

phore; several contractile vacuoles; fresh water.

k). Lorica 80-1 50/z long body 20-25/x by axopodia 50/x long. Genus Chrysosphaerella Lauterborn. In spherical colony, individual cell, oval or pyriform, with 2 chromatophores; imbedded in

P. cyrtophora L. CFig. 104,

18-25ju;

gelatinous mass fresh water.

;

I). Individuals up to 15^ by 9^; colony up to 250ju in diameter; in standing water rich in vegetation. Genus Porochrysis Pascher. Shell with several pores through which rhizopodia are extended a flagellum passes through an apical

C. longispina L. (Fig. 104,

pore; a single small chromatophore; leucosin; a contractile vacuole;

fresh water.

MASTIGOPHORA, CHRYSOMONADINA

261

P. aspergillus P. (Fig. 105, c, d). Shell about 35m long by 25/z wide; chromatophore very small; a large leucosin grain; fresh water. Genus Myxochrysis Pascher. Body multinucleate, amoeboid; with yellowish moniliform chromatophores, many leucosin granules and contractile vacuoles; holozoic; surrounded by a brownish envelop which conforms with body form; flagellated swarmers develop into

Fig. 105. a, flagellate and b, amoeboid phase of Chrysamoeba radians, (Klebs); c, surface view and d, optical section of Porochrysis aspergillus, X400 (Pascher); e-j, Myxochrysis paradoxa (Pascher). e, a medium large Plasmodium with characteristic envelop; the large food vacuole contains protophytan, Scenedesmus, X830; f, diagrammatic side view of a Plasmodium, engulfing a diatom; moniliform bodies are yellowish chromatophores, X1000; g-i, development of swarmer into Plasmodium (stippled bodies are chromatophores), X1200.

X670

multinucleate Plasmodium; plasmotomy and plasmogamy; fresh

water (Pascher, 1916a).

M. paradoxa

P. (Fig. 105, e-j).

Plasmodium 15-18^

or

more

in

diameter; in standing water.

Genus Angulochrysis Lackey. Body ovoid: colorless, thin lorica rounded anteriorly and flattened posteriorly into "wings"; a single flagellum long; no cytostome; two bright yellow-brown chromatophores; no stigma; swims with a slow rotation; marine (Lackey,
1940).

262

PROTOZOOLOGY

A. erratica L. (Fig. 106, b, c). Body up to 12/x long; lorica up to 30m high; flagellum about four times the body length; Woods Hole. Genus Stylochromonas L. Body ovoid, sessile with a stiff stalk: with a large collar at anterior end; a single flagellum; two golden brown chromatophores; no stigma; marine (Lackey, 1940). S. minuta L. (Fig. 106, d). Body 5-8 m long; collar about 6/x high; flagellum about twice the body length.

Fig. 106. a, Microglena ovum, X680 (Conrad); b, c, two views of Angulochrysis erratica, X900 (Lackey); d, Stylochromonas minuta, X1200 (Lackey).

Family 2 Syncryptidae Poche

Solitary or colonial chrysomonads with 2 equal flagella; with or
pellicle (when present, often sculptured) some possess stalk. Genus Syncrypta Ehrenberg. Spherical colonies; individuals with 2 lateral chromatophores, embedded in a gelatinous mass; 2 con-

without

tractile vacuoles ;

S. volvox E. (Fig. 107, a).

eter; in standing water.

without stigma cysts unknown fresh water. 8-14 M by 7-12/z; colony 20-70m in diam; ;

soidal colony

Genus Synura Ehrenberg (Synuropsis Schiller). Spherical or ellipcomposed of 2-50 ovoid individuals arranged radially; body usually covered by short bristles; 2 chromatophores lateral; no stigma; asexual reproduction of individuals is by longitudinal division; that of colony by bipartition; cysts spherical; fresh water.
Species (Korshikov, 1929).
S. uvella E. (Fig. 107, b). Cells oval; bristles conspicuous;

20-40m

by 8-17^; colony 100-400^

in diameter;

if

present in large numbers,

MASTIGOPHORA, CHRYSOMONADINA
the organism
is

263

said to be responsible for an odor of the water re-

sembling that of ripe cucumber. S. adamsi Smith (Fig., 107 c). Spherical colony with individuals
radiating; individuals long spindle, 42-47/t

by

6.5-7// ; 2 flagella

up

to 17// long; in fresh water pond.

Fig. 107.
(Stein);
c, e,

a,

S.

(Klebs);
(Stokes);

Syncrypta volvox, X430 (Stein); b, Synura uvella, adamsi, X280 (Smith); d, Hymenomonas roseola, Derepyxis amphora, X540 (Stokes); f, D. ollula,

X500 X400 X600

g,

Stylochrysallis parasitica,

X430

(Stein).

Genus Hymenomonas

Stein.

Solitary; ellipsoid to cylindrical;

membrane brownish,

often sculptured; 2 chromatophores; without

stigma; a contractile vacuole anterior; fresh water.

H. roseola S. (Fig. 107, d). 17-50// by 10-20/*. Genus Derepyxis Stokes. With cellulose lorica, with or without a short stalk; body ellipsoid to spherical with 1-2 chromatophores;
2 equal flagella; fresh water.

D. amphora
D. ollula

S. (Fig. 107, e).

Lorica 25-30// by 9-18//; on algae in

15//.

standing water.
S. (Fig. 107,/).

Lorica 20-25// by

Genus Stylochrysalis

Stein.

Body

fusiform; with a gelatinous

stalk attached to Volvocidae; 2 equal flagella; 2 chromatophores;

without stigma; fresh water.

S. parasitica S. (Fig. 107, g).

Body 9-1 l/i

long; stalk about 15/z

long; on

phytomonads.

264

PROTOZOOLOGY
Family 3 Ochromonadidae Pascher

With 2 unequal

flagella;

no

pellicle

and

plastic; contractile

vacu-

oles simple; with or without a delicate test; solitary or colonial;

free-swimming or attached. Genus Ochromonas Wyssotzki. Solitary or colonial; body surface delicate; posterior end often drawn out for attachment; 1-2 chromatophores; usually with a stigma; encystment; fresh water. Many
species (Doflein, 1921, 1923).

0. mutdbilis Klebs (Fig. 108, a).

Ovoid to spherical;

plastic,

15-30m

by 8-22 M

0. ludibunda Pascher (Fig. 108, b).

Not

plastic;

12-17m by 6 12ju.

0. granulans Doflein.

No stigma;

5-12/z long (Doflein, 1922).

Fig. 108. a, Ochromonas mutdbilis, X670 (Senn); b, 0. ludibunda, X540 (Pascher); c, Uroglena volvox, X430 (Stein); d, Uroglenopsis americana, X470 (Lemmermann) e, Cyclonexis annularis, X540 (Stokes); f, Dinobryon sertularia, X670 (Scherffel) g, Hyalobryon ramosum., X540 (Lauterborn); h, Stylopyxis viucicola, X470 (Bolochonzew).
;
;

MASTIGOPHORA, CHRYSOMONADINA

265

Genus Uroglena Ehrenberg. Spherical or ovoidal colon}', composed of ovoid or ellipsoidal individuals arranged on periphery of a gelatinous mass; all individuals connected with one another by gelatinous processes running inward and meeting at a point; with a stigma and a plate-like chromatophore; asexual reproduction of individuals by longitudinal fission, that of colony by bipartition; cysts spherical with spinous projections, and a long tubular process;
fresh water.

One

species.
c).

U. volvox E. (Fig. 108,

in

Cells 12-20/*

by

8-13/*; colony 40-400/*

diameter; in standing water.

Genus Uroglenopsis Lemmermann. Similar

individuals without inner connecting processes.

to

Uroglena,

but

U. americana (Calkins) (Fig. 108, d). Each cell with one chromatophore; 5-8/* long; flagellum up to 32/* long; colony up to 300/* in diameter; when present in abundance, the organism gives an offensive odor to the water (Calkins). Morphology, development
(Troitzkaja, 1924).

U. europaea Pascher.

Similar to the last-named species; but

to 7/* long; colon y 150-300/* in diameter. Genus Cyclonexis Stokes. Wheel-like colony, composed of 10-20 wedge-shaped individuals; young colony funnel-shaped; chromatophores 2, lateral; no stigma; reproduction and encystment unknown
2; cells

chromatophores

up

fresh water.
C. annularis S. (Fig. 108,
e).

Cells 11-14/* long; colony 25-30/* in

diameter; in marshy water with sphagnum.

Genus Dinobryon Ehrenberg. Solitary or

colonial; individuals

with vase-like, hyaline, but sometimes, yellowish cellulose test, drawn out at its base; elongated and attached to the base of test with its attenuated posterior tip; 1-2 lateral chromatophores;

by binary fission; one daughter individuals leaving test as a swarmer, to form a new one; in colonial forms daughter individuals remain attached to the inner margin of aperture of parent tests and there secrete new tests; encystment common; the spherical cysts possess a short process; Ahlstrom (1937) studied variability of North American species and found the organisms occur more commonly in alkaline regions than
usually with a stigma; asexual reproduction
of the

elsewhere; fresh water.

Numerous

species.

D. sertularia E. (Fig. 108,/). 23-43/* by 10-14/*. D. divergens Imhof. 26-65/* long; great variation
calities.

in different lo-

Genus Hyalobryon Lauterborn. Solitary or colonial; individual body structure similar to that of Dinobryon; lorica in some cases

266
tubular,

PROTOZOOLOGY
and those
;

of

young individuals are attached

to the exterior

of parent tests fresh water.

H. ramosum L.
ter;

(Fig. 108, g). Lorica 50-7 0/j long by 5-9 ^ in diamebody up to 30/x by 5/x; on vegetation in standing fresh water. Genus Stylopyxis Bolochonzew. Solitary; body located at bottom

of a delicate stalked lorica with a

wide aperture 2 lateral chromato;

phores fresh water.

;

S. mucicolali. (Fig. 108, h). Lorica

17 18^ long; stalk about

33/x

long;

body 9 llyu

long: fresh water.

Family 4 Coccolithidae Lohmann

The members of this family occur, with a few exceptions, in salt water only; with perforate (tremalith) or imperforate (discolith) discs, composed of calcium carbonate; 1-2 flagella; 2 yellowish

a, Pontosphaerahaeckeli, X1070 (Kiihn); b, DiscosphaeratubiX670 (Klihn); c, Distephanus speculum, X530 (Kiihn); d, Rhizochrysis scherffeli, X670 (Doflein); e-g, Hy drums foetidus (e, entire colony; f, portion; g, cyst), e (Berthold), f, X330, g, X800 (Klebs); h, i, Chrysocapsa paludosa, X530 (West); j, k, Phaeosphaera gelatinosa (j, part

Fig. 109.

fer,

of a

mass,

X 70

k, three cells,

X330) (West).

MASTIGOPHORA, CHRYSOMONADINA
;

267

chromatophores a single nucleus; oil drops and leucosin; holophytic. Taxonomy and phylogeny (Schiller, 1925, 1926; Conrad, 1928a;

Kamptner, 1928; Deflandre, 1952a).

Examples
Pontosphaera haeckeli

Lohmann

(Fig. 109, a).

b).

Discosphaera tubifer Murray and Blackman (Fig. 109,

Family 5

Silicoflagellidae Borgert

Exclusively marine planktons; with siliceous skeleton which envelops the body. Example: Distephanus speculum (Miiller) (Fig. 109,
c)

(Deflandre, 1952).

Suborder 2 Rhizochrysidina Pascher

No flagellate stage is known to occur; the organism possesses pseudopodia; highly provisional group, based wholly upon the absence of
flagella;

naked or with

test; various

forms; in some species chroma-

tophores are entirely lacking, so that the organisms resemble some

members of the Sarcodina. Several genera. Genus Rhizochrysis Pascher. Body naked and amoeboid with 1-2
;

chromatophores fresh water.

:

R. scherffeli P. (Figs. 109, d; 110,

a, b).

10-14/* in diameter; 1-2

chromatophores: branching rhizopods; fresh water.

eral in linear association

Genus Chrysidiastrum Lauterborn. Naked; spherical; often sevby pseudopodia; one yellow-brown chroC. catenation L. Cells 12-14ju in diameter (Pascher, 1916a).

matophore; fresh water.

Genus Chrysarachnion Pascher. Ameboid organism; with achromatophore, leucosin grain and contractile vacuole; many individuals arranged in a plane and connected by extremely fine rhizopods, the whole forming a cobweb network. Small animals are trapped by the net; chromatophores are small; nutrition both holophytic and holoduring division the chromatophore is often unevenly distributed so that many individuals without any chromatophore are produced; fresh water (Pascher, 1916a).
zoic;

C. insidians P. (Fig. 110,

in

c,

d).

Highly amoeboid individuals 3-4/x

diameter; chromatophore pale yellowish brown, but becomes blu-

ish green

upon death

of

organisms; a leucosin grain and a contractile

calcareous

vacuole; colony

made up of 200 or more individuals. Genus Chrysothylakion Pascher. With retort-shaped

with a bent neck and an opening;
shell reddish

shell

brown (with

268

PROTOZOOLOGY

Fig. 110. a, b, Rhizochrysis scherffeli, X500 (Scherffel). a, 4 chromatophore-bearing individuals and an individual without chromatophore; b, the last-mentioned individual after 7 hours, c, d, Chrysarachnion insidians (Pascher). c, part of a colony composed of individuals with and without chromatophore, X1270; d, products of division, one individual lacks chromatophore, but with a leucosin body, X2530. e, f, Chrysothylakion vorax (Pascher). e, an individual with anastomosing rhizopodia and "excretion granules," XS70; f, optical section of an individual; the cytoplasm contains two fusiform brownish chromatophores, a spheroid nucleus, a large leucosin body and contractile vacuole, X about 1200.

MASTIGOPHORA, CHRYSOMONADINA
iron) in old individuals;
fine

269

through the aperture are extruded extremely anastomosing rhizopods; protoplasm which fills the shell is colorless; a single nucleus, two spindle-form brown chromatophores, several contractile vacuoles and leucosin body; marine water. C. vorax P. (Fig. 110, e, /). The shell measures 14-18/x long, 7-10/x broad, and 5-6/x high; on marine algae.

Suborder 3 Chrysocapsina Pascher

Palmella stage prominent; flagellate forms transient; colonial; mass 1-2 flagella, one chromato;

individuals enclosed in a gelatinous

phore, and a contractile vacuole; one group of relatively minute

forms and the other

of large organisms.

Genus Hydrurus Agardh. In a

ellipsoidal;

large (1-30 cm. long) branching

gelatinous cylindrical mass; cells yellowish brown; spherical to

gelatinous matrix; apical growth resembles
tiplication of

with a chromatophore; individuals arranged loosely in much higher algae; mulindividuals results in formation of pyrimidal forms

with a flagellum, a chromatophore, and a leucosin mass; cyst show a wing-like rim; cold freshwater streams.

may

H. foetidus Kirschner
occasionally encrusted

(Figs. 32, d-f; 109, e-g). Olive-green, feath-

ery tufts, 1-30 cm. long, develops an offensive odor; sticky to touch;

with calcium carbonate; in running fresh

water.

Genus Chrysocapsa Pascher. In a spherical to ellipsoidal gelatinous mass; cells spherical to ellipsoid; 1-2 chromatophores; with or without stigma freshwater. C. paludosa P. (Fig. 109, h, i). Spherical or ellipsoidal with cells distributed without order; with a stigma; 2 chromatophores; s warmer pyriform with 2 flagella; cells llju long; colony up to 100/z
;

in diameter.

Genus Phaeosphaera West and West. In a simple

tophore; fresh water.
P. gelatinosa

or branching

cylindrical gelatinous mass; cells spherical with a single

chroma-

W. and W.

(Fig. 109, j, k). Cells 14-17.5/x in diameter.

References

Butschli, O. (1883-1887) Mastigophora. Bronn's Klassen und Ord:

nungen des Thierreichs. 1, pt. 2. Doflein, F. and Reichenow, E. (1949) Lehrbuch der Protozoen:

Jena. Grasse, P.-P.: (1952) Traite de Zoologie.

1.

kunde. 6th ed.

S.:

I.

Fasc.

1.

Paris.

Kent,

(1880-1882)

manual

of Infusoria.

London.

270

PROTOZOOLOGY
Teil. In:

Pascher, A.: (1914) Flagellatae: Allgemeiner

serflora Deutschlands. Part
zig1.

Die Siisswas-

Stein, F.: (1878) Der Organismus der Infusionsthiere. 3 Abt. Leip(1883)

Der Organismus der

Leipzig.

Flagellate oder Geisselinfusorien.

Parts

1, 2.

Ahlstrom, E. H.: (1936) The deep-water plankton

of

Lake Michi-

gan, exclusive of the Crustacea. Tr. Am. Micr. Soc, 55:286. (1937) Studies on variability in the genus Dinobryon. Ibid., 56:139. Conrad, W.: (1926) Recherches sur les flagellates de nos eaux saumatres. II. Arch. Protist., 56:167. (1927) Essai d'une monographie des genres Mallomonas Perty (1852) et Pseudomallomonas Chodat (1920). Ibid., 59:
423. (1928)
58.

Le genre Microglena. Ibid., 60:415. (1928a) Sur les Coccolithophoracees d'eau douce. Ibid., 63:

(1930) Flagellates nouveaux ou peu connus. I. Ibid., 70:657. (1952) Classe des Silicoflagellides. In: Grasse (1952), p. 425. (1952a) Classe des Coccolithophorides. Ibid., p. 440. Doflein, F.: (1921) Mitteilungen liber Chrysomonadien aus dem Schwarzwald. Zool. Anz., 53:153. (1922) Untersuchungen liber Chrysomonadinen. I, II. Arch. Protist., 44:149. (1923) III. Ibid., 45:267. Fritsch, F. E.: (1935) The structure and reproduction of the algae.

Deflandre, G.:

Cambridge.
A.: (1952) Classe des Chrysomonadines. In: Grasse (1952), p. 471. Kamptner, E.: (1928) Ueber das System und die Phylogenie der Kalkflagellaten. Arch. Protist., 64: 19. Korshikov, A. A.: (1929) Studies on the chrysomonads. I. Ibid., 67: 253. Lackey, J. B. (1938) Scioto River forms of Chrysococcus. Am. Mid-

Hollande,

land Natur., 20:619.

- (1940) 23:463.
66:50. (1949)

Some new flagellates from

the

Woods Hole
I.

area. Ibid.,

Owen,'h. M.:

(1947) Flagellar structure.

68: 261.

Tr.

Am.

Micr. Soc,

II. Ibid.,

Pascher, A.: (1916) Studien

liber die rhizopodiale Flagellaten. Arch. Protist., 36:81.

Entwicklung der

(1916a) Rhizopodialnetz als Fangvorrichtung bei einer plasmodialen Chrysomonade. Ibid., 37:15. (1916b) Fusionsplasmodien bei Flagellaten und ihre Bedeutung fur die Ableitung der Rhizopoden von den Flagellaten.
Ibid., 37:31.

MASTIGOPHORA, CHRYSOMONADINA

271

und Rhizopoden in ihren gegenseitigen 38:584. oder wenig bekannte Protisten. Ibid., 44:119. (1921) (1929) XXI. Ibid., 65:426. Scherffel, A.: (1901) Kleiner Beitrag zur Phylogenie einiger Gruppen niederer Organismen. Bot. Zeit., 59:143. (1927) Beitrag zur Kenntnis der Chrysomonadineen. II. Arch. Protist., 57:331. Schiller, J.: (1925) Die planktonischen Vegetationen des adriatischen Meeres. A. Ibid., 51:1. (1925a) B. Ibid., 53:59. (1926) Ueber Fortpflanzung, geissellose Gattungen und die Nomenklatur der Coccolithophoraceen, etc. Ibid., 53:326. (1926a) Der thermische Einfluss und die Wirkung des Eises auf die planktischen Herbstvegetationen, etc. Ibid., 56:1. (1929) Neue Chryso- und Cryptomonaden aus Altwassern der Donau bei Wien. Ibid., 66:436. Smith, G. M.: (1950) The freshwater algae of the United States. 2 ed. New York. Stokes, A. C.: (1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71.
(1917) Flagellaten
Ibid.,

Beziehungen. Neue

Troitzkaja, O. V.: (1924) Zur Morphologie und Entwicklungsge-

West, G.

von Uroglenopsis americana. Arch. Protist., 49:260. and Fritsch, F. E.: (1927) A treatise on the British freshwater algae. Cambridge.
schichte
S.

Chapter

Order 2 Cryptomonadina Stein

cryptomonads THE constant body form.
the body
is

differ

from the chrysomonads in having a Pseudopodia are very rarely formed, as

pellicle.

covered by a

The majority show

dorso-ventral

an oblique longitudinal furrow. 1-2 unequal flagella arise from the furrow or from the cytopharynx. In case 2 flagella are present, both may be directed anteriorly or one posteriorly. These organisms are free-swimming or creeping. One or two chromatophores are usually present. They are discoid or band-form. The color of chromatophores varies: yellow, brown, red, olive-green; the nature of the pigment is not well understood, but it is said to be similar to that which is found in the Dinoflagellata (Pascher). One or more spherical pyrenoids which are enclosed within a starch envelope appear to occur outside the chromatophores. Nutrition is mostly holophytic; a few are saprozoic or holozoic. Assimilation products are solid discoid carbohydrates which stain blue with iodine in Cryptomonas or which stain reddish violet by iodine in Cryptochrysis fat and starch are produced in holozoic forms which feed upon bacteria and small Protozoa. The stigma is usually located near the insertion point of the flagella. Contractile vacuoles, one to several, are simple and are situated near the
differentiation, with
;

cytopharynx. A single vesicular nucleus is ordinarily located near the middle of the body. Asexual reproduction, by longitudinal fission, takes place in either the active or the non-motile stage. Sexual reproduction is unknown. Some cryptomonads form palmella stage and others gelatinous aggregates. In the suborder Phaeocapsina, the palmella stage is

permanent. Cysts are spherical, and the cyst wall

cellulose.

is

composed

of

The Cryptomonadina occur

in fresh or sea water, living

also often as symbionts in

marine organisms.
Suborder 1 Eucryptomonadina Suborder 2 Phaeocapsina (p. 275)

Flagellate forms predominant

Palmella stage permanent

Suborder

Eucryptomonadina Pascher

Truncate anteriorly; 2 anterior flagella; with an oblique furrow near Family 1 Cryptomonadidae (p. 273) anterior end Reniform; with 2 lateral flagella; furrow equatorial Family 2 Nephroselmidae (p. 274)
272

CRYPTOMONADINA
Family
cle; anterior
1

273

Cryptomonadidae Stein
Elliptical

Genus Cryptomonas Ehrenberg.

end truncate, with 2

body with a

firm pelli-

flagella; dorsal side

convex, ventral

side slightly so or flat; nucleus posterior;

ules,

"cytopharynx" with gran-

considered trichocysts by some observers (Hollande, 1942, 1952); 2 lateral chromatophores vary in color from green to blue-

brown or rarely red; holophytic; with small starch-like bodies which stain blue in iodine; 1-3 contractile vacuoles anterior; fresh water. Several species. Morphology and taxonomy (Hollande, 1942,
green,
1952).

Fig. 111. a, Cryptomonas ovata, X800 (Pascher);b, Chilomonas Paramecium, X1330 (Biitschli); c, d, Chrysidella schaudinni, X1330 (Winter); e, Cyathomonas truncata, X670 (Ulehla); f, Cryptochrysis commutata, X670 (Pascher); g, Rhodomonas lens, X1330 (Ruttner); h, Nephroselmis olvacea, X670 (Pascher) i, Protochrysis phaeophycearum, X800 (Pascher); j, k, Phaeothamnion confervicolum, X600 (Kiihn).
;

C. ovata E. (Fig. Ill, a). 30-60/x by 20-25/x; among vegetation. Genus Chilomonas Ehrenberg. Similar to Cryptomonas in general body form and structure, but colorless because of the absence of

chromatophores; without pyrenoid; "cytopharynx" deep, lower half surrounded by granules, considered by Hollande (1942) and Dragesco (1951) as trichocysts; one contractile vacuole anterior; nucleus in posterior half; endoplasm usually filled with polygonal starch
grains; saprozoic fresh water.
C.

Paramecium E.

(Fig. 111,6). Posteriorly

narrowed, slightly bent

in stag-

"dorsally"; 30-40 m

by 10-1 5m; saprozoic; widely distributed

274

PROTOZOOLOGY

nant water. Cytology (Mast and Doyle, 1935; Hollande, 1942; Dragesco, 1951); bacteria-free culture (Mast and Pace, 1933); metabolism (Mast and Pace, 1929; Pace, 1941); growth substances (Pace, 1944, 1947; Mast and Pace, 1946); effects of vitamins (Pace,
1947).
C. oblonga Pascher. Oblong; posterior
50/i long.

end broadly rounded; 20similar to Cryptomonas-

Genus Chrysidella Pascher. Somewhat

but

yellow chromatophores much shorter; those oc, curring in Foraminifera or Radiolaria as symbionts are known as

much

smaller-,

Zooxanthellae. Several species.

C. schaudinni (Winter) (Fig. Ill,
c,

d).

Body

less

than 10m long;

in

the foraminiferan Peneroplis pertusus.

Genus Cyathomonas Fromentel. Body small, somewhat oval; without chromatophores; much compressed; anterior end obliquely truncate; with 2 equal or subequal anterior flagella; colorless; nucleus central; anabolic products, stained red or reddish violet by
iodine; contractile vacuole usually anterior; a

row

of refractile

granules, protrichocysts, close

and

parallel to anterior

margin

of

body; asexual reproduction by longitudinal fission; holozoic; nant water and infusion. One species. C. truncata Ehrenberg (Fig. Ill, e). 15-25ju by 10-15/i.

in stag-

Genus Cryptochrysis Pascher. Furrow indistinctly granulated; 2 or more chromatophores brownish, olive-green, or dark green, rarely red; pyrenoid central; 2 equal flagella; some lose flagella and

may assume amoeboid form

C.

fresh water.

commutataV. (Fig. Ill, /). Bean-shaped; 2 chromatophores; 19/x by 10m. Genus Rhodomonas Karsten. Furrow granulated; chromatophore one, red (upon degeneration the coloring matter becomes dissolved
in water)
;

pyrenoid central fresh water.

;

R. lens Pascher and Ruttner (Fig. Ill,

long; in fresh water.

g).

Spindle-form; about 16m

Family 2 Nephroselmidae Pascher

Body reniform; with lateral equatorial furrow; 2 flagella arising from furrow, one directed anteriorly and the other posteriorly. Genus Nephroselmis Stein. Reniform; flattened; furrow and cytopharynx distinct; no stigma; 1-2 chromatophores, discoid, brownish green; nucleus dorsal; a central pyrenoid; 2 contractile
vacuoles; with reddish globules; fresh water.

N. olvacea

S. (Fig. Ill, h).

20-25m by 15m-

CRYPTOMONADINA
Genus
tinct furrow,

275

Protochrysis Pascher. Reniform; not flattened; with a dis-

but without cytopharynx; a stigma at base of flagella; 1-2 chromatophores, brownish yellow; pyrenoid central; 2 contractile vacuoles fission seems to take place during the resting stage
;

fresh water.

P. phaeophycearum P. (Fig. Ill,

i).

15-17/z

by

7-9//.

Suborder 2 Phaeocapsina Pascher

Palmella stage predominant; perhaps border-line forms between

brown algae and cryptomonads. Example: Phaeothamnion vicolum Lagerheim (Fig. Ill, j, k) which is less than 10// long.
References

confer-

(1951) Sur la structure des trichocystes du flagelle cryptomonadine, Chilomonas paramecium. Bull. micr. appl., 2 ser. 1:172. Fritsch, F. E. (1935) The structure and reproduction of the algae.

Dragesco,

J.:

Cambridge.

Hollande,

flagell^s libres.

Etude cytologique et biologique de quelques Arch. zool. exper. gn., 83:1. (1952) Classe des Cryptomonadines. In: Grasse (1952), p.
A.: (1942)

286.

Mast,

S. O. and Doyle, W. L.: (1935) A new type of cytoplasmic structure in the flagellate Chilomonas paramecium. Arch.Protist., 85:145. and Pace, D. M. (1933) Synthesis from inorganic compound of starch, fats, proteins and protoplasm in the colorless animal,
:

Chilomonas paramecium. Protoplasma, 20:326. (1939) The effect of calcium and magnesium on metabolic processes in Chilomonas. J. Cell. Comp. Physiol., 14:
261.

(1946) The nature of the growth-substance produced by Chilomonas paramecium. Physiol. Zool., 19:223. Pace, D. M.: (1941) The effects of sodium and potassium on metabolic processes in Chilomonas paramecium. J. Cell. Comp.

between concentration of growth-promoting substance and its effect on growth in Chilomonas paramecium. Physiol. Zool., 17:278. (1947) The effects of vitamins and growth-promoting substance on growth in Chilomonas paramecium. Exper. Med. Surg.
5:140.

Physiol., 18:243. (1944) The relation

Pascher, A.: (1913) Cryptomonadinae. Susswasserflora Deutschlands. 2.

West, G.

S. and Fritsch, F. E.: (1927) freshwater algae. Cambridge.

treatise

on the British

Chapter

10

Order 3 Phytomonadina Blochmann

THE

small, more or less rounded, green flagelwith a close resemblance to the algae. They show a definite body form, and most of them possess a cellulose membrane, which is thick in some and thin in others. There is a distinct opening in the membrane at the anterior end, through which 1-2 (or 4 or more) flagella protrude. The majority possess numerous grass-green chromatophores, each of which contains one or more pyrenoids. The method of nutrition is mostly holophytic or mixotrophic; some colorless forms are, however, saprozoic. The metabolic products are usually starch and oils. Some plr^tomonads are stained red, owing to the presence of haematochrome. The contractile vacuoles may be located in the anterior part or scattered throughout the body. The nucleus is ordinarily centrally located, and its division seems to be mitotic, chromosomes having been definitely noted in several species. Asexual reproduction is by longitudinal fission, and the daughter individuals remain within the parent membrane for some time. Sexual reproduction seems to occur widely. Colony formation also occurs, especially in the family Volvocidae. Encystment and formation of the palmella stage are common among many forms. The phytomonads have a much wider distribution in fresh than in salt

phytomonads are

lates,

water.
Solitary

Membrane
2 3 4 5 6
flagella flagella flagella flagella

a single piece; rarely indistinct

or

more

flagella

Membrane

bivalve

Family 1 Chlamydomonadidae Family 2 Trichlorididae (p. 281) Family 3 Carteriidae (p. 281) Family 4 Chlorasteridae (p. 283) Family 5 Polyblepharididae (p. 284) Family 6 Phacotidae (p. 284)
(1

Colonial, of 4 or

more individuals; 2

or 4) flagella Family 7 Volvocidae (p. 285)

Family

Chlamydomonadidae Butschli

Solitary; spheroid, oval, or ellipsoid; with a cellulose

membrane;

2 flagella; chromatophores, stigma, and pyrenoids usually present.

Cytology (Hollande, 1942). Genus Chlamydomonas Ehrenberg. Spherical, ovoid or elongated; sometimes flattened; 2 flagella; membrane often thickened at anterior end; a large chromatophore, containing one or more pyrenoids;
276

PHYTOMONADINA

277

stigma; a single nucleus; 2 contractile vacuoles anterior; asexual

reproduction and palmella formation; sexual reproduction isogamy

or anisogamy; fresh water.

Numerous

species (Pascher, 1921, 1925,

1929, 1930, 1932: Skvortzow, 1929; Pringsheim, 1930; Pascher

and

Jahoda, 1928; Moewus, 1932, 1933; Gerloff, 1940); variation (Moewus, 1933) sexual development (Moewus, 1933a) variation (p. 223)
; ;

genetics (p. 231).

C. monadina Stein (Fig. 112, a-c). 15-30/x long; fresh water; Landacre noted that the organisms obstructed the sand filters used in connection with a septic tank, together with the diatom Navicula.
C. angulosa Dill. C. epiphytica C. globosa

About 20^u by 12-15/z; fresh water. Smith (Fig. 112, d). 8-9/j, by 7-8/*; in freshwater lakes.
(Fig. 112, e).

Snow

Spheroid or ellipsoid; 5-7 n in dia-

meter; in freshwater lakes.

by 5-7 n; fresh water. Genus Haematococcus Agardh (Sphaerella Sommerfeldt). SpheC. gracilis S. (Fig. 112,/). 10-13/x

chromatophore peripheral with 2-8 scattered pyrenoids; several contractile vacuoles; haematochrome frequently abundant in both motile and encysted stages; asexual reproduction in motile form; sexual reproduction isogamy; fresh water. H. pluvialis (Flotow) (Figs. 42; 112, g). Spherical; with numerous radial cytoplasmic processes; chromatophore U-shape in optical section; body 8-50m, stigma fusiform, lateral; fresh water. Reichenow (1909) noticed the disappearance of haematochrome if the culture medium was rich in nitrogen and phosphorus. In bacteria-free cultures, Elliott (1934) observed 4 types of cells: large and small flagellates, palmella stage and haemato cysts. Large flagellates predominate
roidal or ovoid with a gelatinous envelope
reticulate,
;

and

in liquid cultures,

but when conditions become unfavorable, palmella

stage and then haematocysts develop.

When

the cysts are placed in

etc.,

a favorable environment after exposure to freezing, desiccation,

they give

rise to

small flagellates which grow into palmella stage or

large flagellates.

No syngamy of small flagellates was noticed. Haematochrome appears during certain phases in sunlight and its appearance is accelerated by sodium acetate under sunlight. Sexuality
(Schulze, 1927).

Genus Sphaerellopsis Korschikoff (Chlamydococcus

gelatinous envelope which
is

Stein).

With

usually ellipsoid with rounded ends;

body elongate fusiform

or pyriform,

no protoplasmic processes to

envelope; 2 equally long flagella; chromatophore large; a pyrenoid;

with or without stigma; nucleus in anterior half; 2 contractile vacuoles; fresh water.

278

PROTOZOOLOGY
14-30/zby 10-20m; fresh water.
processes,

S. fluviatilis (Stein) (Fig. 112, h).

Genus Brachiomonas Bohlin. Lobate; with horn-like

all

directed posteriorly; contractile vacuoles; ill-defined chromato-

phore; pyrenoids; with or without stigma; sexual and asexual reproduction; fresh, brackish or salt water.

Fig. 112. a-c, Chlamydomonas monadina, X470 (Goroschankin) (a, typical organism; b, anisogamy; c, palmella stage); d, C. epiphytica, X1030 (Smith); e, C. globosa, X2000 (Snow); f, C. gracilis, X770 (Snow);
g,

Haematococcus

pluvialis,

X500 (Reichenow);
i,

h, Sphaerellopsis fluvia-

tilis,

X960 (West); j, Diplostauron pentagonium, X1110 (Hazen); 1, Gigantochloris permaxima, X370 (Pascher); m, Gloeomonas ovalis, X330 (Pascher); n, Scourfieldia complanata, X1540 (West); o,
(Korschikoff);

X490

Brachiomonas westiana,
k,

Lobomonas

rostrata,

X1335 (Hazen);

Thorakomonas sabulosa, X670 (Korschikoff).

PHYTOMONADINA
B. westiana Pascher (Fig. 112,
water.
i).

279

15-24/t

by

13-23/z; brackish

Genus Lobomonas Dangeard. Ovoid or irregularly angular; chro matophore cup-shaped; pyrenoid; stigma; a contractile vacuole,
fresh water.

L. rostrata Hazen (Fig. 112, j). 5-12 /i by 4-8 /*. Genus Diplostauron Korschikoff. Rectangular with

raised cor-

ners; 2 equally long flagella; chromatophore; one pyrenoid; stigma;

2 contractile vacuoles anterior; fresh water.

D. pentagonium (Hazen)
in size

(Fig. 112, k). 10-13/*

Genus Gigantochloris Pascher. Unusually

ellipsoid in profile;

by 9 10mlarge form, equalling

a colony of Eudorina; flattened; oval in front view; elongate membrane radially striated; 2 flagella widely

apart, less than

body length; chromatophore

in

network; numerous

pyrenoids; often without stigma; in woodland pools.

permaxima P. (Fig. 1 12, 1). 70-150/* by 40-80/x by 25-50/*. Genus Gloeomonas Klebs. Broadly ovoid, nearly subspherical; with a delicate membrane and a thin gelatinous envelope; 2 flagella
G.

widely apart; chromatophores numerous, circular or oval discs;

pyrenoids
G. ovalis

(?);

stigma; 2 contractile vacuoles anterior; freshwater.

(Fig. 112, m). 38-42/x

K.

by

23-33/*; gelatinous envelope

over

2/*

thick.

flattened; ovoid in front 2-5 times body length; a chromatophore; without pyrenoid or stigma; contractile vacuole anter-

Genus Scourfieldia West. Whole body

view;
ior;

membrane

delicate; 2 flagella

nucleus central; fresh water.

;

S.

complanata W. (Fig. 112, n). 5.2-5. 7/* by 4. 4-4. 6m fresh water. Genus Thorakomonas Korschikoff. Flattened; somewhat irregu-

larly

shaped or

ellipsoid in front view;

membrane

thick, enclustered

with iron-bearing material, deep brown to black in color; protoplasmic body similar to that of Chlamydomonas; a chromatophore
with a pyrenoid; 2 contractile vacuoles; standing fresh water.
T. sabulosa

K.

(Fig. 112, o).

Up

to 16//

by

14/*.

Genus Coccomonas

Stein. Shell

smooth; globular; body not

filling

intracapsular space; stigma; contractile vacuole; asexual reproduction into 4 individuals fresh water. Species
;

(Conrad 1930).

C. orbicularis S. (Fig. 113, a). 18-25/1 in diameter; fresh water.

Genus Chlorogonium Ehrenberg. Fusiform; membrane thin and

adheres closely to protoplasmic body; plate-like chromatophores
usually present, sometimes ill-contoured; one or more pyrenoids; numerous scattered contractile vacuoles; usually a stigma; a central nucleus; asexual reproduction by 2 successive transverse fissions

280

PROTOZOOLOGY

during the motile phase; isogamy reported; fresh water. during the motile phase; isogamy reported; fresh water. Sexuality
(Schulze, 1927); nutrition (Loefer, 1935).
b). 25-70/1 by 4-1 5/x; in stagnant water. Genus Phyllomonas Korschikoff. Extremely flattened membrane delicate; 2 flagella; chromatophore often faded or indistinct; numer-

C. euchlorum E. (Fig. 113,

ous pyrenoids; with or without stigma;

fresh water.

many

contractile vacuoles;

c, Phyllomonas phacoides, X200 (KorSphaenochloris printzi, X600 (Printz); e, Korschikoffia guttula, X1670 (Pascher); f, Fur cilia lobosa, X670 (Stokes); g, Hyalogonium klebsi, X470 (Klebs); h, Polytoma uvella, X670 (Dangeard); i, Parapolytoma satura, X1600 (Jameson); j, Trichloris paradoxa, X990 (Pascher).

Fig. 113. euchlorum,

schikoff);

a,

Coccomonas

orbicularis,

X500

(Stein); b,

Chlorogonium

X430 (Jacobsen);

d,

P. phacoides K. (Fig. 113,

100/i long; in

c).

Leaf -like; rotation movement; up to

standing fresh water.

late

Genus Sphaenochloris Pascher. Body truncate or concave at flagelend in front view; sharply pointed in profile; 2 flagella widely

apart; chromatophore large; pyrenoid; stigma; contractile vacuole

anterior; fresh water.

Up to 18/x by 9/*. Genus Korschikoffia Pascher. Elongate pyriform with an undulating outline; anterior end narrow, posterior end more bluntly
S. printzi P. (Fig. 113, d).

rounded; plastic; chromatophores in posterior half; stigma absent; contractile vacuole anterior; 2 equally long flagella; nucleus nearly
central salt water.
;

PHYTOMONADINA
K. guttula P.

281

Genus
side view

(Fig. 113, e). 6-lOyu by 5m; brackish water. Furcilla Stokes. U-shape, with 2 posterior processes; in

somewhat

flattened; anterior

end with a papilla; 2

oil

flagella

equally long; 1-2 contractile vacuoles anterior;

water.

droplets; fresh

F. lobosa S. (Fig. 113,/). 11-14 M long; fresh water.

Genus Hyalogonium Pascher. Elongate spindle-form anterior end

;

bluntly rounded; posterior end more pointed; 2 flagella; protoplasm colorless; with starch granules; a stigma; asexual reproduction results in

up to 8 daughter

cells;

fresh water.

by up to 10m; stagnant water. Genus Polytoma Ehrenberg (Chlamydoblepharis France; Tussetia Pascher). Ovoid; no chromatophores; membrane yellowish to
H.
klebsi P. (Fig. 113, g). 30-80/x

brown; pyrenoid unobserved; 2 contractile vacuoles; 2 flagella about body length; stigma if present, red or pale-colored; many starch bodies and oil droplets in posterior half of body; asexual reproduction in motile stage; isogamy (Dogiel, 1935); saprozoic; in
stagnant fresh water. Genetics
P. uvella E. (Figs.
(p. 231).

may

Oval to pyriform; stigma be absent; 15-30/x by 9-20m- Cytology (Entz, 1918; Hollande,
8, c; 97, a, b; 113, h).

1942).

Genus Parapolytoma Jameson. Anterior margin obliquely truncryptomonad, but without chromatophores; without stigma and starch; division into 4 individuals within envelope;
cate, resembling a

fresh water.

P. satura

J. (Fig. 113, i).

About 15m by

10m; fresh water.

Family 2 Trichlorididae

and Pascher. Bean-shape; flagellate chromatophore large, covering convex side; 2 pyrenoids surrounded by starch granules; a stigma near posterior end of chromatophore; nucleus central; numerous contractile vacuoles scattered; 3 flagella near

Genus

Trichloris Scherffel

side flattened or concave; opposite side convex;

anterior end.
T.

paradoxa S and P.

(Fig. 113, j). 12-15/x

broad by 10-12 M high;

flagella

up to 30m

long.

Family 3 Carteriidae

Genus Carteria Diesing (Corbierea, Pithiscus Dangeard). Ovoid, chromatophore cup-shaped; pyrenoid; stigma; 2 contractile vacuoles;
fresh water.

Numerous

species (Pascher, 1925, 1932; Schiller, 1925).

282

PROTOZOOLOGY
Heart-shaped
in front view;

C. cordiformis (Carter) (Fig. 114, a).

ovoid in profile; chromatophore large; 18-23/x by 16-20/t. C. ellipsoidalis Bold. Ellipsoid; chromatophore; a small stigma; division into 2, 4, or 8 individuals in encysted stage; 6-24/x long;
fresh water,
Stein). Small pyramidal or heart-shaped body; with bluntly drawn-out posterior end; usually 4 ridges in anterior region; 4 flagella; green chromatophore cup-shaped; with or without stigma; a large pyrenoid in the

Maryland (Bold, 1938). Genus Pyramimonas Schmarda (Pyramidomonas

posterior part; 2 contractile vacuoles in the anterior portion ;'encyst-

ment; fresh water. Several species

P. tetrarhynchus S. (Fig. 114,

(Geitler, 1925).

b).

20-28/*

by

12-18/*; fresh water;

Wisconsin (Smith, 1933).

Fig. 114. a, Carteria cordiformis, X600 (Dill); b, Pyramimonas tetrarhynchus, X400 (Dill); c, d, Polytomella agilis, X1000 (Doflein) (d, a cyst) e, Spirogonium chlorogonioides, X 670 (Pascher) /, Tetrablepharis 7nultifilis, X670 (Pascher); g, Spermatozopsis exultans, XI 630 (Pascher); h, Chloraster gyrans, X670 (Stein); i, Polyblepharides singularis, X870 (Dangeard); j, k, Pocillomonas flos aquae, X920 (Steinecke); 1, m, Phacotus lenticularis, X430 (Stein); nj Pteromonas angulosa, X670 (West); o, p, Dysmorphococcus variabilis, X1000 (Bold).
; ;

PHYTOMONADINA

283

P. montana Geitler. Bluntly conical; anterior end 4-lobed or

truncate; posterior end narrowly rounded; plastic; pyriform nucleus
anterior, closely associated with 4 flagella; stigma; 2 contractile

vacuoles anterior; chromatophore cup-shaped, granular, with scattered starch grains and oil droplets a pyrenoid with a ring of small
;

starch grains;

17-22.5/1

long (Geitler,

1925);

12-20/*

(Bold); flagella about

1938).

body length;

fresh water,

by 8-16/* Maryland (Bold,

Genus Polytomella Aragao.

Ellipsoid, or oval, with a small papilla

;

at anterior end, where 4 equally long flagella arise

with or without

stigma; starch: fresh water (Aragao, 1910; Doflein, 1916).

P. agilis A. (Fig. 114,
c,

d).

Numerous

starch grains; 818/*

by

5-9/*; flagella 12-17/* long; fresh

water; hay infusion.

P. caeca Pringsheim. Ovoid with bluntly pointed posterior end;

by 10-12/*; membrane delicate; a small papilla at anterior end; no stigma; two contractile vacuoles below papilla; cytoplasm ordinarily filled with starch grains; fresh water (Pringsheim, 1937).
12-20/*

Genus Medusochloris Pascher. Hollowed hemisphere with 4 proceach bearing a flagellum at its lower edge; a lobed plateshaped chromatophore; without pyrenoid. One species. M. phiale P. In salt water pools with decaying algae in the Baltic. Genus Spirogonium Pascher. Body spindle-form; membrane delicate; flagella a little longer than body; chromatophore conspicuous; a pyrenoid; stigma anterior; 2 contractile vacuoles; fresh water. One
esses,

species. S. chlorogonioides (P). (Fig. 114, e).

Body up

to 25/*

by

15/*.

Genus Tetrablepharis Senn.

fresh water.

Ellipsoid to ovoid; pyrenoid present;

T. multifilis (Klebs) (Fig. 114,/). 12-20/* by 8-15/*; stagnant water. Genus Spermatozopsis Korschikoff. Sickle-form; bent easily, oc-

casionally plastic; chromatophore mostly on convex side; a distinct stigma at more rounded anterior end; flagella equally long; 2 contractile vacuoles anterior; fresh water infusion. S. exultans K. (Fig. 114, g). 7-9/* long; also biflagellate in fresh water with algae, leaves, etc.
;

Family 4 Chlorasteridae

Genus Chloraster Ehrenberg. Similar to Pyramimonas, but anterior half with a conical envelope drawn out at four corners; with 5
flagella; fresh or salt water.

C. gyrans E. (Fig. 114, h).

Up

to 18/* long; standing water; also re-

ported from salt water.

284

PROTOZOOLOGY
Family 5 Polyblepharididae Dangeard

shorter than
fresh water.

Genus Polyblepharides Dangeard. Ellipsoid or ovoid; flagella 6-8, body length; chromatophore; a pyrenoid; a central

nucleus; 2 contractile vacuoles anterior; cysts; a questionable genus;

i). 10-14 M by 8-9/x. Genus Pocillomonas Steinecke. Ovoid with broadly concave anterior end; covered with gelatinous substance with numerous small

P. singularis D. (Fig. 114,

projections; 6 flagella; chromatophores disc-shaped;

2 contractile

vacuoles anterior; nucleus central; starch bodies; without pyrenoid.

P.flos aquae S. (Fig. 114, j, k). 13m

by

10m; fresh water pools.

Family 6 Phacotidae Poche

The

shell typically

anterior end; with stigma

within the shell

composed of 2 valves; 2 flagella protrude from and chromatophores; asexual reproduction valves may become separated from each other ow-

ing to an increase in gelatinous contents.

in profile;

Genus Phacotus Perty. Oval to circular in front view; lenticular protoplasmic body does not fill dark-colored shell comthrough a foramen; asexual reproduction
m). 13-20m in diameter; in
of suture
;

pletely; flagella protrude

into 2 to 8 individuals fresh water.

P. lenticularis (Ehrenberg) (Fig. 114, stagnant water.

I,

Genus Pteromonas
of

Seligo.

Body broadly winged in plane

fills

2 valves; protoplasmic body

shell;

chromatophore cup-

shaped; one or more pyrenoids; stigma; 2 contractile vacuoles; asexual reproduction into 2-4 individuals; sexual reproduction by isogamy; zygotes usually brown; fresh water. Several species.
P. angulosa
water.

(Lemmermann)

(Fig. 114, n).

and 4 protoplasmic projections

in profile; 13-17/i

With a rounded wing by 9-20m; fresh

Genus Dysmorphococcus Takeda. Circular

in front view; anterior

region narrowed; posterior end broad; shell distinctly flattened posteriorly, ornamented by numerous pores; sutural ridge without
pores; 2 flagella; 2 contractile vacuoles; stigma, pyrenoid, cup-shaped chromatophore; nucleus; multiplication by binary fission; fresh

water.

D. variabilis T. (Fig. 114, o, p). Shell 14-19/x by 13-17/x; older dark brown; fresh water; Maryland (Bold, 1938).

shells

PHYTOMONADINA
Family 7 Volvocidae Ehrenberg

285

An

interesting group of colonial flagellates; individual similar to

sphaera; 4 in Spondylomorum)

flagella (one in Mastigogreen chromatophores, pyrenoids, stigma, and contractile vacuoles; body covered by a cellulose mem,

Chlamydomonadidae, with 2 equally long

brane and not plastic; colony or coenobium

exclusively freshwater inhabitants.

is

discoid or spherical;

Genus Volvox Linnaeus. Often large spherical or subspherical number of cells which are differentiated into somatic and reproductive cells; somatic cells numerous, embedded in gelatinous matrix, and contains a chromatophore, one or more pyrenoids, a stigma, 2 flagella and several contractile vacuoles; in some species cytoplasmic connection occurs between adjacent cells; generative cells few and large. Reproduction is by
colonies, consisting of a large

parthenogenesis or true sexual fusion. In parthenogenetic colonies,

the gametes are larger in size and fewer in
(Fig. 77)

number

as

the macrogametes of the female colonies. Sexual fusion

compared with is anisogamy

and sexual colonies

may

be monoecious or dioecious. Zy-

by a smooth, ridged or spinous wall. Fresh water. Many species. Smith (1944) made a comprehensive study of 18 species on which the following species descriptions are based. V. globator L. (Fig. 115, a, b). Monoecious. Sexual colonies 350500m in diameter; 5000-15,000 cells, with cytoplasmic connections; 3-7 microgametocytes, each of which develops into over 250 microgametes; 10-40 macrogametes; zygotes 35-45/1 in diameter, covered with many spines with rounded tip. Parthenogenetic colonies 400GOO/i in diameter; 4-10 gametes, 10-13/i in diameter; young colonies up to 250/i. Europe and North America. V. aureus Ehrenberg (Figs. 77; 115, c-e). Dioecious. Male colonies 300-350/* in diameter; 1000-1500 cells, with cytoplasmic connections; numerous microgametocytes; clusters of some 32 microgametes, 15-18/x in diameter. Female colonies 300-400/*; 2000-3000 cells; 10-14 macrogametes; zygotes 40-60/x with smooth surface. Parthenogenetic colonies up to 500/z; 4-12 gametes; young colonies 150/x in diameter. Europe and North America. Sexual differentiation (Mainx, 1929). V. tertius Meyer. Dioecious. Male colonies up to 170/t in diameter; 180-500 cells, without cytoplasmic connections; about 50 microgametocytes. Female colonies up to 500ju; 500-2000 cells; 2-12 macrogametes; zygotes 60-65/i with smooth wall. Parthenogenetic

gotes are usually yellowish to brownish red in color and covered

286

PROTOZOOLOGY

^oo o o oo o.o
.<;-/

o ooocS?:

o
D

of

o"W

Ns(

%&

Fig. 115. Species of Volvox ("Smith), a, b, Volvox globator (a, a female colony, X150; b, a zygote, X370); c-e, V. aureus (c, a young parthenogenetic colony; d, a mature male colony, X125; e, a zygote, X370); f-h, V. spermatosphaera: f, a parthenogenetic colony, X185; g, a mature male colony, X370; h, a zygote, X370); i, a zygote of V. weismannia, X370; j, k, V. per globator (j, a male colony, XI 50; k, a zygote, X370).

PHYTOMONADINA
colonies

287

up to 600 m in diameter; 500-2000 cells; 2-12 gametes. Europe and North America. V. spermatosphaera Powers (Fig. 115, f-h). Dioecious. Male colonies up to 100m in diameter; cells, without connection, up to 128 microgametocytes. Female colonies up to 500 n in diameter; 6-16 macrogametes; zygotes 35-45/1, with smooth membrane. Parthenogenetic colonies up to 650/x in diameter; 8-10 gametes; young colonies ellipsoid, up to 100 ju in diameter. North America (Powers, 1908). V. weismannia P. (Fig. 115, i). Male colonies 100-150/z in diameter; 250-500 cells; 6-50 microgametocytes; clusters of microgametes (up to 128) discoid, 12-15/t in diameter. Female colonies up to 400/*; 2000-3000 cells; 8-24 macrogametes; zygotes 30-50ju in diameter, with reticulate ridges on shell. Parthenogenetic colonies up to 400/z; 1500-3000 cells; 8 or 10 gametes; 40-60/x in diameter; young colonies 1 00-200 /x in diameter. North America (Powers, 1908). V. perglobator P. (Fig. 115, j, k). Dioecious. Male colonies 300450/x in diameter 5000-10,000 cells, with delicate cytoplasmic con-

nections; 60-80 microgametocytes. Female colonies 300-550/z in diameter; 9000-13,000 cells; 50-120 macrogametes; zygotes 30-34/x, covered with bluntly pointed spines. Parthenogenetic colonies as
large as 1.1

mm;

three to nine gametes;

young

colonies 250-275/x in

diameter. North America.

Miiller. 4 or 16 individuals arranged in one plane; ovoid or slightly polygonal; with 2 flagella arranged in the plane of coenobium; with or without a gelatinous envelope; protoplasmic
cell

Genus Gonium

connections

among individuals occur occasionally; asexual reproduc-

tion through simultaneous divisions of

component cells; sexual reproduction isogamy; zygotes reddish; fresh water. Colony formation
(Hartmann, 1924).
G. sociale (Dujardin) (Fig. 116, a). 4 individuals

colony; cells 10-22/*

lakes.

by

6-16// wide; in

form a discoid open waters of ponds and

G. pectorale

M.

(Fig. 116, b). 16 (rarely 4 or 8) individuals

form a

colony; 4 cells in center; 12 peripheral, closely arranged; cells 5-14/x

by

10/x;

colony up to

90/z in

diameter; fresh water.

G. /orraoswm Pascher. 16 cells in a colony further apart; peripheral

gelatinous envelope reduced; cells similar in size to those of G. so-

but colony somewhat larger; freshwater lakes. Genus Stephanoon Schewiakoff. Spherical or ellipsoidal colony, surrounded by gelatinous envelope, and composed of 8 or 16 biciale

288
flagellate cells,

PROTOZOOLOGY
arranged in 2 alternating rows on equatorial plane;
16 individuals in ellipsoidal colony;
30/t long;

fresh water.
S. askenasii S. (Fig. 117, a).
cells 9/x in

diameter; flagella up to

Genus Platydorina Kofoid. 32

plane; flagella

colony 78/* by 60/zarranged in a slightly twisted directed alternately to both sides; dioecious; fresh
cells

water.

P. caudata K. (Fig. 117, b). Individual cells 10-15/t long; colony up to 165m long by 145ju wide, and 25/u thick; dioecious; anisogamy; macrogametes escape from female colonies and remain attached to

Fig. 116.

a,

Gonium
torale,

sociale,

X270 CChodat); X670 CHartmann).

b, G. pec-

them or swim about until fertilized by microgametes; zygotes become thickly walled (Taft, 1940). Genus Spondylomorum Ehrenberg. 16 cells in a compact group in 4 transverse rings; each with 4 flagella; asexual reproduction by simultaneous division of component cells; fresh water. One species. S. quaternarium E. (Fig. 117, c). Cells 12-26/x by 8-15/i; colony up to 60ju long. Genus Chlamydobotrys Korschikoff. Colony composed of 8 or 16 individuals; cells with 2 flagella; chromatophore; stigma no
;

pyrenoid; fresh water. Species (Pascher, 1925); culture (Schulze,

1927).
C. stellata

K.

(Fig.

117, d).

Colony composed

of 8 individuals
in

arranged in 2 rings; individuals 14-15m long; colony 30-40/1 diameter; Maryland (Bold, 1933).

PHYTOMONADINA

289

Genus Stephanosphaera Cohn. Spherical or subspherical colony, with 8 (rarely 4 or 16) cells arranged in a ring; cells pyriform, but with several processes; 2 flagella on one face; asexual reproduction
and isogamy
(p.

183) fresh water.

;

Fig. 117.

a,

Stephanoon askenasii, X440 (Schewiakoff);

c,
;

b,

Platydorina

caudata,

Spondylomorum quaternarium, X330 (Stein); d, Chlamydobotrys stellata, X430 (Korschikoff) e, Stephanosphaera pluvialis, X250 (Hieronymus) f, Pandorina morum, X300 (Smith); g, h, Eudorina elegans, X310 Mastigosphaera gobii, X520 (Schewiakoff (Goebel); i, Pleodorina illinoisensis, X200 (Kofoid).
;

X2S0 (Kofoid);

7-13m long; colony 30-60/x Culture and sexuality (Schulze, 1927). Genus Pandorina Bory. Spherical or subspherical colony of usually 16 (sometimes 8 or 32) biflagellate individuals, closely packed
S. pluvialis C. (Figs. 80; 117, e). Cells
in diameter.

within a gelatinous, but firm and thick matrix; individuals often

angular; with stigma and chromatophores; asexual reproduction

290

PROTOZOOLOGY

through simultaneous division of component individuals; anisogamy; zygotes colored and covered by a smooth wall; fresh water. One species.
P.
40/x,

morum

(Miiller) (Figs. 117, /). Cells 8-17/z long; colony

20-

up to 250/z in diameter; ponds and ditches. Genus Mastigosphaera Schewiakoff. Similar to Pandorina; but individuals with a single flagellum which is 3.5 times the body length;
fresh water.

M.

gobii S. (Fig. 117, g). Individual 9m long; colony 30-33/*.

Genus Eudorina Ehrenberg. Spherical

or ellipsoidal colony of

usually 32 or sometimes 16 spherical cells; asexual reproduction

similar to that of Pandorina; sexual reproduction with 32-64 spheri-

macrogametes and numerous clustered microgametes which unite with the macrogametes within the colony; reddish zygotes with a smooth wall; fresh water. Colony formation (Hartmann, 1924). E. elegans E. (Fig. 117, h). Cells 10-24^ in diameter; colony 40150 fx in diameter; in ponds, ditches and lakes. Culture and morphology (Hartmann, 1921); response to light (Luntz, 1935). Genus Pleodorina Shaw. Somewhat similar to Eudorina, being composed of 32, 64, or 128 ovoid or spherical cells of 2 types: small somatic and large generative, located within a gelatinous matrix;
cal green

when mature,

Sexual reproduction similar to that of Eudorina; fresh water. P. illinoisensis Kofoid (Figs. 32, b, c; 117, i). 32 cells in ellipsoid
colony, 4 vegetative

and 28 reproductive individuals; arranged

cells

in

5 circles, 4 in each polar circle, 8 at equator and 8 on either side of

equator; 4 small vegetative

at anterior pole; vegetative cells

10-16/x in diameter; reproductive cells 19-25/x in diameter; colony

up to 160m by

130/z.
cells,

P. californica S. Spherical colony with 64 or 128

of

which

1/2-2/3 are reproductive cells; vegetative cells 13-1 5m; reproductive cells up to 27/x; colony up to 450/x, both in diameter. Variation (Tiffany, 1935); in Ukraine (Swirenko, 1926).

References

Aragao, H.

Untersuchungen iiber Polytomella agilis n.g., n. sp. Mem. Inst. Oswaldo Cruz, 2:42. Bold, H. C: (1938) Notes on Maryland algae. Bull. Torrey Bot.
B.: (1910)

Club., 65:293.

Conrad, W. (1930)
:

Flagellates

nouveaux ou peu connus.

I.

Arch.

Protist., 70:657.

Crow, W.

domonads.

B.: (1918) The classification of New Phytol., 17:151.

some

colonial

Chlamy-

PHYTOMONADINA
Dangeard, P.: (1900) Observations ment du Pandorina morum. Le

291

sur la structure et le developpeBotaniste, 7:192. Doflein, F.: (1916) Polytomella agilis. Zool. Anz., 47:273. Dogiel, V.: (1935) Le mode de conjugaison de Polytoma uvella. Arch. zool. exper. gen., 77 (N. et R.) 1:1. Elliott, A. M.: (1934) Morphology and life history of Haematococcus pluvialis. Arch. Protist., 82:250. Entz, G. Jr.: (1913) Cytologische Beobachtungen an Polytoma uvella. Verh. deutsch. zool. Ges. Ver. Berlin, 23:249. (1918) Ueber die mitotische Teilung von Polytoma uvella.
:

Arch. Protist., 38:324. Fritsch, F. E.: (1935) The structure and reproduction of the algae. Geitler, L.: (1925) Zur Kenntnis der Gattung Pyramidoraonas. Arch. Protist., 52:356. Gerloff, J.: (1940) Beitrage zur Kenntnis der Variabilitat und Systematik der Gattung Chlamydomonas. Ibid., 94:311. Harper, R. A.: (1912) The structure and development of the colony in Gonium. Tr. Am. Micr. Soc, 31:65.
(1921) Untersuchungen iiber die Morphologie und Physiologie des Formwechsels der Phytomonadien. III. Arch. Protist., 43:223. (1924) Ueber die Veranderung der Koloniebildung von Eudorina elegans und Gonium pectorale unter dem Einfluss ausserer Bedingungen. IV. Ibid., 49:375. Hollande, A.: (1942) Etude cytologique et biologique de queleques flagelles libres. Arch. zool. exper. gen., 83:1. Janet, C.: (1912, 1922, 1923) Le Volvox. I. II and III Memoires.

Hartmann, M.:

Kofoid, C. A.: (1900) Plankton studies.

Hist., Ser.

II, III.

Ann. Mag. Nat,

7,6:139.

Loefer,

J. B.: (1935) Effect of certain carbohydrates and organic acids on growth of Chlorogonium and Cbilomonas. Arch Protist.,
(

compounds on growth of Chlorogonium and Chilomonas. Ibid., 85:74. Luntz, A.: (1935) Ueber die Regulation der Reizbeantwortung bei

84:456. 1935a) Effect of certain nitrogen

Mainx,

koloniebildenden griinen Einzelligen. Ibid., 86:90. F.: (1929) Ueber die Geschlechterverteilung bei Volvox aureus. Ibid., 67:205. Mast, S. O.: (1928) Structure and function of the eye-spot in unicellular and colonial organisms. Ibid., 60:197. Moewus, F.: (1932) Neue Chlamydomonaden. Ibid., 75:284.

iiber die Sexualitat und Entwick(1933a) lung von Chlorophyceen. Ibid., 80:469. Pascher, A.: (1921) Neue oder wenig bekannte Protisten. Arch. Protist., 44:119. (1925) Neue oder wenig bekannte Protisten. XVII. Ibid., 51

Untersuchungen domonaden. Untersuchungen

(1933)
Ibid., 80:128.

liber die Variabilitat

von Chlamy-

549.

292
(1925a) XVIII.

PROTOZOOLOGY
Ibid., 52:566.

(1927) Volvocales

Phytomonadinae.

Die Siisswasserflora.

Pt. 4.

(1929) 65:426.

Neue oder wenig bekannte

Protisten. Arch. Protist.,

(1930) Neue Volvocalen. Ibid., 69:103. (1932) Zur Kenntnis der einzelligen Volvocalen. Ibid., 76:1. and Jahoda, Rosa: (1928) Neue Polyblepharidinen und

Chlamydomonadinen aus den Almtumpeln

61:239.

um

Lunz. Ibid.,

J.: (1952) Classe de Phytomonadines ou Volvocales. In: Grasse (1952), p. 154. Powers, J. H.: (1907) New forms of Volvox. Tr. Am. Micr. Soc, 27:123. (1908) Further studies in Volvox with descriptions of three

Pavillard,

new

species.

Ibid., 28: 141.

etc.

Pringsheim, E. G.: (1930) Neue Chlamydomonadaceen,

Arch.

Protist., 69:95.

(1937) Zur Kenntnis saprotropher Algen

und

Flagellaten. II.

Ibid., 88:151.

Reichenow, E.: (1909) Untersuchungen an Haematococcus pulvialis nebst Bemerkungen iiber andere Flagellaten. Arb. kaiserl.
Gesundh., 33:1. Schiller, J.: (1925) Die planktonischen Vegetationen des adriatischen Meeres. B. Arch. Protist., 53:59. Schulze, B.: (1927) Zur Kenntnis einiger Volvocales. Ibid., 58: 508. Shaw, W. R.: (1894) Pleodorina, a new genus of the Volvocideae. Bot. Gaz., 19:279. Skvortzow, B. W. (1929) Einige neue und wenig bekannte Chlamydomonadaceae aus Manchuria. Arch. Protist., 66:160. Smith, G. M.: (1944) A comparative study of the species of Volvox. Tr. Am. Micr. Soc, 63:265. (1950) The freshwater algae of the United States. New York. Swirenko: (1926) Ueber einige neue und interessante Volvocineae, etc. Arch. Protist., 55:191. Taft, C. E. (1940) Asexual and sexual reproduction in Platydorina caudata. Tr. Am. Micr. Soc, 59:1. Tiffany. L. H.: (1935) Homothallism and other variations in Pleodorina californica. Arch. Protist., 85:140. West, G. S. and Fritsch, F. E.: (1927) A treatise on the British freshwater algae. Cambridge.
:
:

Chapter

11

Order 4 Euglenoidina Blochmann

THE body body

is

some are plastic, others have a form with a well-developed, striated or variously sculptured pellicle. At the anterior end, there is an opening through which a flagellum protrudes. In holophytic forms the so-called cytostome and cytopharynx, if present, are apparently not concerned with the food-taking, but seem to give a passage-way for the flagellum and also to excrete the waste fluid matters which become collected in one or more contractile vacuoles located near the reservoir. In holozoic forms, a well-developed cytostome and cytopharynx are present. Ordinarily there is only one flagellum, but some possess two or three. Chromatophores are present in the majority of the Euglenidae, but absent in two families. They are green, vary in
as a rule elongated;
definite

shape,

such

as

spheroidal,

band-form,

cup-form,

discoidal,

or

fusiform,

and usually possess pyrenoids. Some forms may contain haematochrome. A small but conspicuous stigma is invariably present near the anterior end of the body in chromatophore-bearing
Reserve food material
of the organism.
is

forms.

the paramylon body,

fat,

and

oil,

the

presence of which depends naturally on the metabolic condition

The paramylon body assumes

is,

diverse forms in dif-

ferent species, but

as a rule, constant in each species,

and

this

a certain extent. Nutrition is holophytic in chromatophore-possessing forms, which, however,

facilitates specific identification to

may be saprozoic, depending on

stances present in the water.
algae,

the

amount

of light

The

holozoic forms feed

and organic subupon bacteria,

and smaller Protozoa.

is, as a rule, large and distinct and contains almost always a large endosome. Asexual reproduction is by longitudinal fission; sexual reproduction has been observed in a few species. Encystment is common. The majority inhabit fresh water, but some live in brackish or salt water, and a few are parasitic in animals. Taxonomy (Mainx, 1928; Hollande, 1942, 1952a); Jahn, 1946; Pring-

The nucleus

sheim, 1950.

With stigma Without stigma With 1 flagellum With 2 flagella

293

Family

Euglenidae

(p.

294)

Family 2 Astasiidae Family 3 Anisonemidae

(p.
(p.

302) 303)

294

PROTOZOOLOGY
Family
1

Euglenidae Stein

Body

plastic ("euglenoid"), but, as a rule,

more

or less spindle-

form during locomotion. The flagellum arises from a blepharoplast located in the cytoplasm at the posterior margin of the reservoir. Between the blepharoplast and the "cytostome," the flagellum shows a swelling which appears to be photosensitive (Mast, 1938). Many
observers consider that the basal portion of the flagellum
is

bifur-

cated and ends in two blepharoplasts, but Hollande (1942), Pringsheim (1948) and others, hold that in addition to a long flagellum

from a blepharoplast, there is present a short flagellum which does not extend beyond the neck of the reservoir and often adheres to the long flagellum, producing the appearance of bifurcation. Culture and physiology (Mainx, 1928); cytology (Giinther, 1928; Holarising

lande, 1942).

Genus Euglena Ehrenberg. Short or elongated spindle, cylindrical, marked by longitudinal or spiral striae; some with a thin pellicle highly plastic; others regularly spirally twisted; stigma usually anterior; chromatophores numerous and
or band-form; pellicle usually
discoid, band-form, or fusiform; pyrenoids

may

or

may

not be sur-

rounded by starch envelope; paramylon bodies which may be two in number, one being located on either side of nucleus, and rod-like to ovoid in shape or numerous and scattered throughout; contractile
vacuole small, near reservoir; asexual reproduction by longitudinal fission; sexual reproduction reported in Euglena sanguined ; common in stagnant water, especially where algae occur; when present in
large numbers, the active organisms

may form a green film on the and resting or encysted stages may produce conspicuous green spots on the bottom of pond or pool; in fresh water.
surface of water

Numerous

species (Pascher, 1925; Johnson, 1944; Gojdics, 1953).

a).

E. pisciformis Klebs (Fig. 118,

20-35/*

by

5-10/*; spindle-form

with bluntly pointed anterior and sharply attenuated posterior end; slightly plastic; a body-length flagellum, active; 2-3 chromatophores; division into two or four individuals in encysted stage
(Johnson, 1944).

E. viridis Ehrenberg (Fig. 118, 6). 40-65/* by 14-20/*; anterior end rounded, posterior end pointed; fusiform during locomotion; highly plastic when stationary; flagellum as long as the body; pellicle obliquely striated; chromatophores

more or

less

bandform, radially

arranged; nucleus posterior; nutrition holophytic, but also saprozoic. Multiplication in thin-walled cysts (Johnson).
E. acus E. (Fig. 118,
c).

50-175/*

by

8-18/*;

body long spindle

or

EUGLENOIDINA

295

cylinder, with a sharply pointed posterior end; flagellum short, about

I the body length; spiral striation of pellicle very delicate; numerous discoid chromatophores; several paramylon bodies, rod-form and

12-20ju long; nucleus central; stigma distinct;

movement

sluggish.

b,

Fig. 118. Species of Euglena (Johnson), a, Euglena pisciformis, X855; E. viridis, X400; c, E. acus, X555; d, E. spirogyra, X460; e, E. oxyuris, X200; f, E. sanguinea, X400; g, E. deses, X315; h, E. gracilis, X865; i, E. tripteris, with optical section of body, X345; j, E. ehrenbergi, X145; k, E. terricola, X345; 1, E. sociabilis, X320; m, two individuals of E.
klebsi,

X335;

n,

two individuals

of E. rubra,

X355.

E. spirogyra E. (Fig. 118,

terior

end a

little

d). 80-125 ;u by 10-35m; cylindrical; annarrowed and rounded, posterior end drawn out;

spiral striae,

made up of small knobs, conspicuous; many discoid chromatophores; two ovoidal paramylon bodies, 18-45/x by 10-18/x, one on either side of centrally located nucleus; flagellum about \ the body length; stigma prominent; sluggish. E. oxyuris Schmarda (Fig. 118, e). 1 50-500 m by 20-40^; cylindri-

296
cal;

PROTOZOOLOGY

almost always twisted, somewhat flattened; anterior end roundend pointed; pellicle with spiral striae; numerous discoid chromatophores; two ovoid paramylon bodies, 20-40/* long, one on either side of nucleus, and also small bodies; stigma large; flageled, posterior

lum

short; sluggish.

E. sanguinea E. (Fig. 118,/). 80-170/* by 25-45/*; posterior end bluntly rounded; flagellum about the body length; pellicle striated;
elongate chromatophores
darkness.
plastic; faint striae;
lie

parallel to the striae;

haematochrome

granules scattered in sun light and collected in the central area in

E. deses E. (Fig. 118, g). 85-170/* by 10-20/*; elongate; highly stigma distinct; nucleus central; chromato-

phores discoid with pyrenoid; several small rod-shaped paramylon

scattered; flagellum less than \ the

body

length.

E. gracilis Klebs (Fig. 118, h). 35-55/* by 6-25/*; cylindrical to elongate oval; highly plastic; flagellum about the body length; fusi-

form chromatophores 10-20; nucleus central; pyrenoids. E. tripteris Dujardin (Fig. 118, i). 70-120/* by 12-16/*; elongate; three-ridged, rounded anteriorly and drawn out posteriorly; pellicle
longitudinally striated; only slightly plastic; stigma prominent; discoid chromatophores numerous;

two paramylon

bodies, rod-shaped

and one on
length.

either side of the nucleus; flagellum about f the

body

E. ehrenbergi Klebs (Fig. 118,

j).

170-400/*

by

15-40/*; cylindrical

end rounded; plastic, often twisted; spiral striation; numerous small discoid chromatophores; stigma conspicuous; 2 paramylon bodies elongate, up to over 100m long; flagellum about \ the body length or less. E. terricola Dangeard (Fig. 118, k). 65-95/* by 8-18/*; pellicle thin and highly plastic; nucleus central; chromatophores long (20-30/*) rods; paramylon bodies small and annular; flagellum about the body length. E. sociabilis D. (Fig. 118, 1). 65-112/* by 15-30/*; cylindrical; delicate pellicle; highly plastic; numerous elongate chromatophores; paramylon bodies discoid; flagellum slightly longer than body. E. klebsi Mainx (Fig. 118, m). 45-85/* by 5-10/*; form highly plastic; chromatophores discoid; paramylon bodies rod-shaped, up
flattened, posterior

and

to several; flagellum short.

E. rubra Hardy (Fig. 118, n). 70-170/* by 25-36/*; cylindrical; rounded anteriorly and drawn out posteriorly; spiral striation; nucleus posterior; flagellum longer than body; stigma about 7/* in diameter; many fusiform chromatophores aligned with the body striae;

EUGLENOIDINA

297

numerous haematochrome granules, 0.3-0.5/x in diameter: ovoid paramylon bodies; reproductive and temporary cysts and protective
34-47^ in diameter, with a gelatinous envelope. Johnson (1939) found that the color of this Euglena was red in the morning and dull green in the late afternoon, due to the difference in the distribution of haematochrome within the body. When haematochrome granules are distributed throughout the body, the organism is bright-red, but when they are condensed in the center of the body, the organism is dull green. When part of the area of the pond was shaded with a board early in the
cysts,

morning, shortly after sunrise all the scum became red except the shaded area. When the board was removed, the red color appeared in 11 minutes while the temperature of the water remained 21C. In the evening the change was reversed. Johnson and Jahn (1942) later found that green-red color change could be induced by raising the temperature of the water to 30-40C. and by irradiation
with infrared rays or visible
function of haematochrome
If this is true, it is

light.

The two workers hold that the

since
it

may be protective,

migrates to a

position which shields the chromatophores from very bright light.

easy to find the species thriving in hot weather in

shallow ponds where temperature of the water rises to 35-45C. In

colder weather,
it

it is

exists in a green phase, containing a

supposed that this Euglena is less abundant and few haematochrome granules.

glena,

Genus Khawkinea Jahn and McKibben. Similar to Genus Eubut without chromatophores and thus permanently colorless
K. halli.L and M. 30-65/z by 12-14/*; fusiform; pellicle spirally than body; stigma 2-3/x in

fresh water.

striated; plastic; flagellum slightly longer

diameter, yellow-orange to reddish-orange, composed of

ules;

many

gran-

numerous (25-100) paramylon bodies elliptical or polyhedral: cysts 20-30^ in diameter; putrid leaf infusion; saprozoic (Jahn and McKibben, 1937). K. ocellata (Khawkine). Similar to above; flagellum 1.5-2 times body length; fresh water. Genus Phacus Dujardin. Highly flattened; asymmetrical; pellicle firm; body form constant; prominent longitudinal or oblique striation; flagellum and a stigma; chromatophores without pyrenoid (Pringsheim) are discoid and green; holophytic fresh water. Numerous species (Skvortzov, 1937; Pochmann, 1942; Conrad, 1943; Allegre and Jahn, 1943); Morphology and cytology (Krichenbauer, 1937;
;

Conrad, 1943).
P. pleuronectes (Miiller) (Fig. 119, a). 45-100 n by 30-70/x; short

298

PROTOZOOLOGY

posterior prolongation slightly curved; a prominent ridge on the convex side, extending to posterior end; longitudinally striated; usually one circular paramylon body near center; flagellum as long as body. P. longicauda (Ehrenberg) (Fig. 119, b). 120-170/* by 45-70/*; usually slightly twisted a long caudal prolongation flagellum about
;

Fig. 119. Species of Phacus (Allegre and Jahn). a, Phacus pleuronedes and an end view, X800; b, P. longicauda, X500; c, P. pyrum and an end view, X880; d, P. acuminata and an end view, XI 300; e, P. monilata, X800; f, P. torta, and an end view, X800; g, P. oscillans, X1400.

one discoidal paramylon body central;

ated.

pellicle longitudinally stri-

P.

pyrum

(E.) (Fig. 119, c).

About 30-50/1 by
two
discoid

10-20/*; circular in

cross-section; with a

medium

long caudal prolongation; pellicle ob-

liquely ridged; stigma inconspicuous;

paramylon bodies;

flagellum as long as the body.

EUGLENOIDINA

299

P. acuminata Stokes (Fig. 119, d). About 30-40 m by 20-30/*; nearly circular in outline; longitudinally striated; usually one small paramylon body; flagellum as long as the body. P. monilata (S) (Fig. 119,
jection; pellicle with
e).

40-55/z

by 32-40/*; a short caudal pro-

minute knobs arranged in longitudinal rows; discoid chromatophores; flagellum about the body length. P. torta Lemmermann (Fig. 119, /). 80-100 m by 40-45/*; body twisted, with a long caudal prolongation; longitudinal striae on pellicle; chromatophores discoid; one large circular paramylon body; flagellum about | the body length. P. oscillans Klebs (Fig. 119, g). 15-35/* by 7-10/x; rounded anteriorly and bluntly pointed posteriorly; striation oblique; 1 or 2 paramylon bodies; flagellum about as long as the body. Genus Lepocinclis Perty (Crumenula Dujardin). Body more or
less ovo-cylindrical; rigid

with spirally striated

pellicle; often

with a

short posterior spinous projection; stigma sometimes present; discoidal chromatophores

numerous and marginal; paramylon bodies

1925,

usually large and ring-shaped, laterally disposed; without pyrenoids;

fresh water.

Many

species (Pascher,

1929: Conrad,

1934;

Skvortzov, 1937).

ovum (Ehrenberg) (Fig. 120, a). Body 20-40 /x long. Genus Trachelomonas Ehrenberg. With a lorica which often possesses numerous spines; sometimes yellowish to dark brown, composed of ferric hydroxide impregnated with a brown manganic compound (Pringsheim, 1948); a single long flagellum protrudes from
L.

the anterior aperture, the rim of which is frequently thickened to form a collar; chromatophores either two curved plates or numerous discs; paramylon bodies small grains; a stigma and pyrenoid; multiplication by fission, one daughter individual retains the lorica and flagellum, while the other escapes and forms a new one; cysts com-

mon;

fresh water. Numerous species (Palmer, 1902, 1905, 1925, 1925a; Pascher, 1924, 1925, 1925a, 1926, 1929; Gordienko, 1929; Conrad, 1932; Skvortzov, 1937; Balech, 1944).

T. hispida (Perty) (Figs. 32, a; 120, b). Lorica oval, with numerous minute spines; brownish; 8-10 chromatophores; 20-42 /i by 15-26/t;

many

varieties.
c).

T. urceolata Stokes (Fig. 120,

Lorica vasiform, smooth with a

short neck; about 45/z long.

T. piscatoris (Fisher) (Fig. 120, d). Lorica cylindrical with a short neck and with numerous short, conical spines; 25-40/z long; flagellum 1-2 times body length.

300

PROTOZOOLOGY
e).
;

T. verrucosa Stokes (Fig. 120,

;

Lorica spherical, with numerous

knob-like attachments no neck 24-25/* in diameter.

T. vermiculosa Palmer (Fig. 120, /). Lorica spherical; with many sausage-form markings; 23m in diameter. Genus Cryptoglena Ehrenberg. Body rigid, flattened; 2 band-form

chromatophores

lateral;

single
species.

flagellum;

nucleus

posterior;

among

freshwater algae.

One

C. pigra E. (Fig. 120, g). Ovoid, pointed posteriorly; flagellum

short; stigma prominent; 10-15/t

by

6-10/t; standing water.

yf+;$$

Ns^jj^

I'/Jf

If]

Fig. 120.

a,

Lepocinclis ovum,
c,

(Stokes); d, T. piscatoris, X520 X550 (Stokes); f, T. vermiculosa, X800 (Palmer); g, Cryptoglena pigra, X430 (Stein); h, Ascoglena vaginicola, X390 (Stein); Eutreptia viridis, X270 (Klebs); j, E. marina, X670 (da Cunha); k, Euglenamorpha hegneri, X730 (Wenrich).
(Stein);
e,

X430

T.

urceolata,

X430 X430

(Stein); b, Trachelomonas hispida,

(Fisher);

T. verrucosa,

i,

Encased in a flexible, colorless to brown base to foreign object; solitary; without stalk; body ovoidal, plastic; attached to test with its posterior end; a single flagellum; a stigma; numerous chromatophores discoid; with or without pyrenoids; reproduction as in Trachelomonas;

Genus Ascoglena

Stein.
its

lorica,

attached with

fresh water.

A. vaginicola S. (Fig. 120, h). Lorica about 43/i by 15/*. Genus Colacium Ehrenberg. Stalked individuals form colony;
frequently attached to animals such as copepods, rotifers, etc. stalk
;

mucilaginous; individual
disco idal chromatophores

cells

pyriform, ellipsoidal or cylindrical;

without flagellum; a single flagellum only in free-swimming stage; numerous; with pyrenoids; multiplication

EUGLENOIDINA
by longitudinal
fission; also

301

by swarmers,

possessing a flagellum and

a stigma; fresh water. Several species.

C. vesiculosum E. (Fig. 121). Solitary or colonial,

made up

of

two

form ovoid to spindle; 22 ju by 12^; seven to ten elongate chromatophores along the periphery; flagellum
to eight individuals; flagellate

Fig. 121. Colacium vesiculosum (Johnson), a, diagram showing the life cycle (a-d, palmella stage; e, formation of flagellate stage; f, formation
of flagellate stage

attached stage);

b, flagellate

by budding of Palmella stage; g, flagellate stage; h, and c, stalked form on a crustacean, X1840.

one to two times the body length; a stigma;

many paramylon bodies;

palmella stage conspicuous; stalked form (Johnson, 1934). Genus Eutreptia Perty (Eutreptiella da Cunha). With 2 flagella at
anterior end; pellicle distinctly striated; plastic; spindle-shaped dur-

ing

oids absent;

movement; stigma; numerous discoid chromatophores; pyrenparamylon bodies spherical or subcylindrical multipli;

cation as in Euglena; cyst with a thick stratified wall; fresh or salt

water.
E. viridis P. (Fig. 120,
i).

50-70 M by 5-13;u;
j).

in fresh water; a

variety was reported from brackish water ponds.

E. marina (da Cunha) (Fig. 120,

Flagella unequal in length;

302

PROTOZOOLOGY
by
8-10/*;

longer one as long as body, shorter one ^; body 40-50/* salt water.
to those of Euglena,
species.

Genus Euglenamorpha Wenrich. Body form and structure

but with 3
flagella; in

similar

gut of frog tadpoles. One

(Wenrich, 1924).

E. hegneri

W.

(Fig. 120, k). 40-50/* long

Family 2 Astasiidae Butschli

body form and general structure, but without chromatophores; body highly plastic, although usually
Similar to Euglenidae in

elongate spindle.

Genus Astasia Dujardin. Body

gate; fresh water or parasitic
(?)

plastic,

although ordinarily elon-

in microcrustaceans.

Many

species

(Pringsheim, 1942). Bacteria-free cultivation (Schoenborn, 1946). A. klebsi Lemmermann (Fig. 122, a). Spindle-form; posterior

Fig.

122. a, Astasia klebsi,

(Stein);
c,

X430
lata,

X1000

X500 (Klebs); b, Urceolus cyclostomus, U. sabulosus, X430 (Stokes); d, Petalomonas mediocanel(Klebs); e, Rhabdomonas incurva, X1400 (Hall); f, ScytoX430
(Stein).

monas

pusilla,

drawn out; flagellum as long as body; bodies oval; 40-50/* by 13-20/*; stagnant water. Genus Urceolus Mereschkowsky (Phialonema
portion
less;

plastic;

paramylon
color-

Stein).

Body

a funnel-like neck; posterior region stout; a single flagellum protrudes from funnel and reaches inward the posterior third of body; fresh or salt water. U. cyclostomus (Stein) (Fig. 122, b). 25-50/* long; fresh water. U. sabulosus (Stokes) (Fig. 122, c). Spindle-form; covered with minute sand-grains; about 58/* long; fresh water.
plastic; flask-shaped; striated;

Genus Petalomonas

Stein.

Oval or pyriform; not

plastic; pellicle

often with straight or spiral furrows; a single flagellum; paramylon

EUGLENOIDINA
bodies; a nucleus; holozoic or saprozoic.

303
species in fresh water

Many

and a few

in salt water. Species

P. mediocanellata S. (Fig.

(Shawhan and Jahn, 1947). 122, d). Ovoid with longitudinal

fur-

flageHum about as long as the body; 21-26/x long. Genus Rhabdomonas Fresenius. Rigid body, cylindrical and not flattened, more or less arched pellicle longitudinally ridged a flagellum through aperture at the anterior tip; fresh water (Pringsheim,

rows on two

sides;

1942). Species (Pascher, 1925); relation to

Menoidium (Pringsheim,

1942).

R. incurva F. (Figs. 69, 122, e). Banana-shaped; longitudinal ridges conspicuous; flagellum as long as the body; 15-25^ by 7-8 n (Hall, 1923); 13-15/x by 5-7;u (Hollande, 1952a); common in standing
water.
Stein. Oval or pyriform, with a delicate pela single flagellum; a contractile vacuole with a reservoir; holozoic on bacteria; longitudinal fission in motile stage; stagnant

Genus Scytomonas

licle;

water and coprozoic.

S. pusilla S. (Fig. 122, /).

About

15/x long.

Cytology

(Schiissler,

1917).

Genus Copromonas Dobell. Elongate ovoid; with a single flagellum; a small cytostome at anterior end; holozoic on bacteria; permanent fusion followed by encystment (p. 183); coprozoic in faecal matters of frog, toad, and man; several authors hold that this genus is probably identical with Scytomonas which was incompletely described

by

Stein.

C. subtilis

D.

(Fig. 78). 7-20ju long. Golgi

body (Gatenby and

Singh, 1938).

Family 3 Anisonemidae Schewiakoff

Colorless

body

plastic or rigid with a variously

marked

pellicle;

2 flagella, one directed anteriorly and the other usually posteriorly;

contractile vacuoles

and

reservoir; stigma absent;

paramylon bodies
less flat-

usually present; free-swimming or creeping.

Genus Anisonema Dujardin. Generally ovoid; more or

tened; asymmetrical; plastic or rigid; a
flagella at anterior
slit-like

ventral furrow;

end; cytopharynx long; contractile vacuole ana).

terior; nucleus posterior; in fresh water. Several species.

A. acinus D. (Fig. 123,

licle slightly striated;

Rigid; oval;
16-22/x.
b).

somewhat

flattened; pel-

25-40m by

A. truncatum Stein (Fig. 123,

20/x.

Rigid; elongate ovoid: 60 m

by

A. emarginatum Stokes (Fig. 123,

c).

Rigid; 14/x long; flagella long.

304

PROTOZOOLOGY

truncate posterior end during locomotion; highly plastic

Genus Peranema Dujardin. Elongate, with a broad rounded or when sta-

tionary; delicate pellicle shows a fine striation; expansible cytostome

with a thickened ridge and two oral rods at anterior end; aperture through which the flagella protrude is also at anterior end; a free flagellum, long and conspicuous, tapers toward free end; a second flagellum adheres to the pellicle; nucleus central; a contractile vacuole, anterior, close

to the reservoir; holozoic; fresh water.

dinarily filled with

d). 4.0-70/x long; body orparamylon or starch grains derived from Astasia, Rhabdomonas, Euglena, etc., which coinhabit the culture; holozoic;

P. trichophorum (Ehrenberg) (Fig. 123,

very
ellar

common

in

stagnant water. Cell inclusion (Hall, 1929); struc-

ture and behavior (Chen, 1950); development (Lackey, 1929); flag-

apparatus (Lackey, 1933; Pitelka, 1945); food intake (Hall, Hyman, 1936; Chen, 1950). P. granulifera Penard. Much smaller in size. 8-1 5ju long; elongate, but plastic; pellicle granulated; standing water. Genus Heteronema Dujardin. Plastic; rounded or elongate; flagella arise from anterior end, one directed forward and the other trailing; cytostome near base of flagella; holozoic; fresh water. Sev1933; Hollande, 1942;
eral species.

H. acus (Ehrenberg) (Fig. 123, e). Extended body tapers towards both ends; anterior flagellum as long as body, trailing one about 1/2; contractile vacuole anterior nucleus central 45-50/* long fresh water. Morphology, reproduction (Loefer, 1931). H. mutabile (Stokes) (Fig. 123,/). Elongate; highly plastic longitudinally striated; about 254/x long; in cypress swamp. Genus Tropidoscyphus Stein. Slightly plastic; pellicle with 8 longitudinal ridges; 2 unequal flagella at anterior pole; holozoic or
; ; ;

saprozoic; fresh or salt water.

T. octocostatus S. (Fig. 123, g). 35-63yu long; fresh water, rich in

vegetation.

Genus Distigma Ehrenberg. Plastic; elongate when extended; body surface without any marking; 2 flagella unequal in length, directed forward; cytostome and cytopharynx located at anterior end; endoplasm usually transparent; holozoic. Several species (Pringsheim, 1942). D. proteus E. (Fig. 123, h). 50-1 10m long when extended; nucleus central; stagnant water; infusion. Cytology (Hollande, 1937). Genus Entosiphon Stein. Oval, flattened; more or less rigid,;
flagella arise from a cytostome, one flagellum trailing; protrusible cytopharynx a long conical tubule almost reaching posterior end;

EUGLENOIDINA
nucleus centro-lateral; fresh water. E. sulcatum (Dujardin) (Fig. 123,
1929, 1929a).
i).

305

About

20/i long

(Lackey,

striae;

ovatum Stokes. Anterior end rounded; 10-12 longitudinal about 25-28/z long. Genus Notosolenus Stokes. Free-swimming; rigid oval; ventral
E.

Fig. 123.
(Stein);
c,

X670;
g,

e,

Anisonema acinus, X400 (Klebs); b, A. truncatum, X430 X530 (Stokes); d, Peranema trichophorum, Heteronema acus, X430 (Stein); f, H. mutabile, XI 20 (Stokes);
a,

A. emerginatum,

Tropidoscyphus octocostatus, X290 (Lemmermann); h, Distigma proteus, X430 (Stein); i, Entosiphon sulcatum, X430 (Stein); j, Notosolenus apocamptus, X120 (Stokes); k, N. sinuatus, X600 (Stokes); 1, m, front and side views of Triangulomonas rigida, X935 (Lackey); n, Marsupiogaster striata, X590 (Schewiakoff ) o, M. picta (Faria, da Cunha and Pinto).
;

306

PROTOZOOLOGY
one long, directed anteriorly and
vibratile;

surface convex, dorsal surface with a broad longitudinal groove;

flagella anterior;

the

other shorter and trailing; fresh water with vegetation. iV. apocamptus S. (Fig. 123, j). Oval with broad posterior end;
6-1 1/x long.

N. sinuatus S. (Fig. 123, h). Posterior end truncate or concave; about 22/t long. Genus Triangulomonas Lackey. Rigid body, triangular, with convex sides; one surface flat, the other elevated near the anterior end; pellicle brownish; a mouth at anterior end with cytopharynx and reservoir: two flagella, one trailing; salt water.
T. rigida L. (Fig. 123,
I,

m).

Body 18m by

15/z;

anterior flagellum

as long as the body; posterior flagellum 1.5 times the

body length;

Woods Hole

(Lackey, 1940). Genus Marsupiogaster Schewiakoff. Oval; flattened; asymmetrical; cytostome occupies entire anterior end; cytopharynx conspicuous, 1/2

body length; body longitudinally

striated; 2 flagella,

one directed anteriorly, the other posteriorly; spherical nucleus;

contractile vacuole anterior; fresh or salt water.

M.

striata

Schewiakoff (Fig. 123, n). About

27/x

by

15/x;

fresh

water; Hawaii.

picta Faria,

da Cunha and Pinto

(Fig. 123, o). In salt water;

Rio de Janeiro.

Order 5 Chloromonadina Klebs

The chloromonads are of rare occurrence and consequently not well known. The majority possess small discoidal grass-green chromatophores with a large amount of xanthophyll which on addition of an acid become blue-green. No pyrenoids occur. The metabolic
products are fatty oil. Starch or allied carbohydrates are absent. Stigma is also not present. Genera (Poisson and Hollande, 1943; Hollande, 1952).

Genus Gonyostomum Diesing (Rhaphidomonas

gle flagellum:
;

Stein).

With a

sin-

chromatophores grass-green; highly refractile trichocyst-like bodies in cytoplasm fresh water. A few species. G. semen D. (Fig. 124, a). Sluggish animal; about 45-60/x long; among decaying vegetation. Genus Vacuolaria Cienkowski (Coelomonas Stein). Highly plastic; without trichocyst-like structures; anterior end narrow; two flagella;

cyst with a gelatinous envelope.

6).

One

species.

V. virescens C. (Fig. 124,

50-70 M by 18-25/*; fresh water. Cy-

tology (Fott, 1935; Poisson and Hollande, 1943).

EUGLENOIDINA, CHLOROMONADINA
Genus Trentonia Stokes.
flattened; anterior
Bi-flagellate as in the last genus;

307

but

margin

slightly bilobed.
c).

One

species.

T. flagellata S. (Fig. 124,

Slow-moving organism; encystment

fresh water.

followed

by binary fission; about 60ju long; Genus Thaumatomastix Lauterborn.

flagella,

Colorless;

pseudo podia
trailing; holo-

formed; 2

one extended anteriorly, the other

Fig. 124. a, Gonyostomum semen, X540 (Stein); b, Vacuolaria virescens, X460 (Senn); c, Trentonia flagellata, X330 (Stokes); d, Thaumatomastix setifera, X830 (Lauterborn)
zoic;

perhaps a transitional form between the Mastigophora and the

Sarcodina.

One

species.

T. setifera L. (Fig. 104, d).

About

20-35/*

by

15-28/*; fresh water.

References

Allegre, C. F. and Jahn, T. L.: (1943) A survey of the genus Phacus Dujardin. Tr. Am. Micr. Soc, 62:233. Balech, E.: (1944) Trachelomonas de la Argentina. An. Mus.
Argent. Cien. Nat., 41:221. T.: (1950) Investigations of the biology of Peranema trichophorum. Quart. J. Micr. Sc, 91:279. Conrad, W.: (1932) Flagellates nouveaux ou peu connus. III. Arch. Protist., 78:463. (1934) Materiaux pour une monographic du genre Lepocinclis. Ibid., 82:203.

Chen, Y.

da

(1943) Notes protistologiques. XXVIII. Bull. Mus. Roy. d'Hist. Natur. Belgique, 19, no. 6. novo genero de "Euglenoidea." Cunha, A. M.: (1913) Sobre Brazil Medico, 27:213.

um

308

PROTOZOOLOGY

Dangeard, P.: (1901) Recherches sur les Eugleniens. La Bot., 8:97. Fott, B.: (1935) Ueber den inneren Bau von Vacuolaria viridis. Arch. Protist., 84:242. Fritsch, F. E.: (1935) The structure and reproduction of the algae. Gatenby, J. B. and Singh, B. N.: (1938) The Golgi apparatus of Copromonas subtilis and Euglena sp. Quart. J. Micr. Sc., 80:567. Gojdics, Mary: (1953) The genus Euglena. Madison, Wisconsin. Gordienko, M.: (1929) Zur Frage der Systematik der Gattung Trachelomonas. Arch. Protist., 65:258. Gunther, F.: (1928) Ueber den Bau und die Lebensweise der Euglenen, etc. Ibid., 60:511. Hall, R. P.: (1923) Morphology and binary fission of Menoidium incurvum. Univ. California Publ. Zool., 20:447. (1929) Reaction of certain cytoplasmic inclusions to vital dyes and their relation to mitochondria and Golgi apparatus in the flagellate Peranema trichophorum. J. Morphol. Physiol., 48:
105.

(1933) (1934)

The method

of ingestion in

Peranema,

etc.

Arch.

Protist., 81:308.

A note on the flagellar apparatus of Peranema, etc. Micr. Soc, 53:237. (1937) A note on behavior of chromosomes. Ibid., 56:288. Hollande, A.: (1937) Quelques donnees nouvelles sur la cytologic d'une Astasiacee peu connu: Distigma proteus. Bull. Soc. zool. Fr., 62:236. (1942) Etudes cytologique et biologique de quelques flagelles libres. Arch. zool. exp. gen., 83:1. (1952) Classe de Chloromonadines. In: Grasse (1952), p. 227. (1952a) Classe des Eugleniens. Ibid., p. 239. Hyman, Libbie H.: (1936) Observations on Protozoa. II. Quart. J. Micr. Sc. 79:50,. Jahn, T. L.: (1946) The euglenoid flagellates. Quart. Rev. Biol., 21:
Tr.

Am.

246.

and

McKibben, W.
:

R.: (1937)

colorless euglenoid flagel-

Khawkinea halli n.g., n.sp. Tr. Am. Micr. Soc, 56:48. Johnson, D. F. (1934) Morphology and life history of Colacium
late,

vesiculosum. Arch. Protist., 83:241. Johnson, L. P.: (1939) study of Euglena rubra. Tr. Soc, 58:42.

Am.

Micr.

color change Euglena rubra. Physiol. Zool, 15:89. Krichenbauer, H.: (1937) Beitrag zur Kenntnis der Morphologie und Entwicklungsgeschichte der Gattungen Euglena und Pha:

(1944) Euglena of Iowa. Ibid., 63:97. and Jahn, T. L. (1942) Cause of the green-red

in

cus. Arch. Protist., 90:88.

Lackey,

J. B.:

(1929) Studies on the

life

history of Euglenida.

I.

Ibid., 66:175.

(1929a) II. Ibid., 67:128. (1933) III. Biol. Bull., 65:238.

EUGLENOIDINA, CHLOROMONADINA
(1940)

309
area.

Some new
E.:

flagellates

from the Woods Hole

Am.

Midi. Nat., 23:463.

(1913) lands. Pt. 2. J. B.: (1931) Morphology and binary fission of Heteronema acus. Arch. Protist., 74:449. Mainx, F. (1928) Beitrage zur Morpholgie und Physiologie der

Lemmermann,

Eugleninae. Siisswasserflora Deutsch-

Loefer,

Eugleninen. I, II. Ibid., 60:305. Palmer, T. C: (1902) Five new species of Trachelomonas. Proc. Acad. Nat. Sc., Philadelphia, 54:791. (1905) Delaware valley forms of Trachelomonas. Ibid., 57:665. (1925) Trachelomonas: etc. Ibid., 77:15. (1925a) Nomenclature of Trachelomonas. Ibid., 77:185. Pascher, A.: (1913) Chloromonadinae. Siisswasserflora Deutsch.
Pt. 2.

(1924)

Neue oder wenig bekannte

Protisten. XIII. Arch.

Protist., 48:492.

(1925) XV. Ibid., 50:486. (1925a) XVII. Ibid., 51:549. (1926) XIX. Ibid., 53:459. (1929) XXI. Ibid., 65:426. Pitelka, Dorothy R. (1945) Morphology and taxonomy of flagellates of the genus Peranema Dujardin. J. Morphol., 76: 179. Pochmann, A.: (1942) Synopsis der Gattung Phacus. Arch. Protist., 95:81. Poisson, R. and Hollande, A.: (1943) Considerations sur la cytologic, la mitose et les affinit^s des Chloromonadies. Ann. Sc. Nat. Ser. Bot. Zool., 5:147. Pringsheim, E. G.: (1942) Contribution to our knowledge of saprophytic Algae and Flagellata. III. New Phytologist, 41:171. (1948) Taxonomic problems in the Euglenineae. Biol. Rev., 23:46. and Hovasse, R. (1948) The loss of chromatophores in Euglena gracilis. New Phytologist, 47:52. (1950) Les relations de parente entre Astasiacees et Euglenacees. Arch. zool. exper. gen., 86:499. Schoenborn, H. W. (1946) Studies on the nutrition of colorless euglenoid flagellates. II. Physiol. Zool., 19:430. Schussler, H.: (1917) Cytologische und entwicklungsgeschichtliche Protozoenstudien. I. Arch. Protist., 38:117. Shawhan, Fae M. and Jahn, T. L.: (1947) A survey of the genus Petalomonas. Tr. Am. Micr. Soc, 66:182. Skvortzov, B. V.: (1937) Contributions to our knowledge of the freshwater algae of Rangoon, Burma, India. I. Arch. Protist., 90:69. Stokes, A. C: (1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71.
:

Chapter

12

Order 6 Dinoflagellata Biitschli

groups the most make one THE Mastigophora, inhabiting mostly marine water, and a
dinoflagellates
of distinct to of the
lesser

extent fresh water. In the general appearance, the arrangement of

the two flagella, the characteristic furrows, and the possession of

brown chromatophores, they are

monadina.

closely related to the Crypto-

The body

may be

is covered by an envelope composed of cellulose which a simple smooth piece, or may be composed of two valves

or of numerous plates, that are variously sculptured and possess

manifold projections. Differences in the position and course of the

furrows and in the projections of the envelope produce numerous asymmetrical forms. The furrows, or grooves, are a transverse annulus and a longitudinal sulcus. The annulus is a girdle around the

middle or toward one end of the body. It may be a complete, incomplete or sometimes spiral ring. While the majority show a single transverse furrow, a few may possess several. The part of the shell anterior to the annulus is called the epitheca and that posterior to the annulus the hypotheca. In case the envelope is not developed, the terms epicone and hypocone are used (Fig. 105). The sulcus may run from end to end or from one end to the annulus. The two flagella arise typically from the furrows, one being transverse and
the other longitudinal.

The transverse flagellum which is often band-form, encircles the body and undergoes undulating movements, which in former years were looked upon as ciliary movements (hence the name Cilioflagellata).

In the suborder Prorocentrinea, this flagellum vibrates freely

in a circle

projects

beyond the body and

flagella

near the anterior end. The longitudinal flagellum often vibrates. Combination of the move-

ments of these

produces whirling movements characteristic

of the organisms.

The majority of dinoflagellates possess a single somewhat massive nucleus with evenly scattered chromatin, and usually several endosomes. There are two kinds of vacuoles. One is often surrounded by a ring of smaller vacuoles, while the other is large, contains pinkcolored fluid and connected with the exterior

by a canal opening

into

a flagellar pore.

The
is

latter is

known

as the pusule which functions

as a digestive organella (Kofoid

forms a stigma

composed

of

and Swezy). In many freshwater and in Pouchetiidae there is an ocellus an amyloid lens and a dark pigment-ball. The majority
present,

310

DINOFLAGELLATA
of planktonic forms possess a large

311

number of small chromatophores which are usually dark yellow, brown or sometimes slightly greenish and are located in the periphery of the body, while bottom-dwelling and parasitic forms are, as a rule, colorless, because of the absence of chromatophores. A few forms contain haematochrome. The method
is

of nutrition

holophytic, holozoic, saprozoic, or mixotrophic. In

oil,

holophytic forms, anabolic products are starch,

Anterior flagellar pore
n.

or fats.

/"
}

-\
\

-Epicone

Annulus or

girdle

^Transverse flagellum
Sulcus

^C

Ls^^^^^^^
\\
4

Hypocone
Longitudinal flagellum

V
-

][r^>j/

of a typical
is

^Posterior

flagellar

pore

Fig. 125.

Diagram

naked dinoflagellate (Lebour).

fission or

Asexual reproduction
groups. Encystment
cyst wall
is

hy binary or multiple
and

budding
different

in either the active or the resting stage

differs

among

is of common occurrence. In some forms the formed within the test. The cysts remain alive for many years; for example, Ceratium cysts were found to retain their vitality in one instance for six and one-half years. Conjugation and sexual fusion have been reported in certain forms, but definite knowledge on

sexual reproduction awaits further investigation.

The

dinoflagellates are

abundant

in the

plankton of the sea and

play an important part in the economy of marine life as a whole. A number of parasitic forms are also known. Their hosts include vari-

ous diatoms, copepods and several pelagic animals. Some dinoflagellates inhabiting various seas multiply suddenly in enormous numbers within certain areas, and bring about distinct discolorations of water, often referred to as "red tide" or "red water." Occasionally the red
of fishes

water causes the death of a large number According to Galtsoff (1948, 1949), the red water which appeared on the west coast of Florida in 1946 and 1947, was due to the presence of an enormous number

and

of various invertebrates.

of

Gymnodinium

brevis

and

this dinoflagellate

seemed

in

some man-

ner to have been closely correlated with the fatal effect on animals entering the discolored water. Ketchum and Keen (1948) found the total phosphorus content of the water containing dense Gymnodinium populations to be 2.5 to 10 times the maximum expected in

312

PROTOZOOLOGY
and throat
irritations in

the sea, and the substance associated with

dinoflagellates causes nose

(1948) observed that similar irritations

Gymnodinium and other man. Woodcock can be produced by breathirritant substance passed

ing air artificially laden with small drops of the red water containing

56X10

dinoflagellates per liter.

The

through a fine bacterial filter, and was found to be very stable, remaining active in stored red water for several weeks. Distribution and taxonomy (Kofoid, 1906, 1907, 1909, 1931; Kofoid and Swezy,
1921; Prescott, 1928; Eddy, 1930; Playfair, 1919; Wailes, 1934;

Thompson,

1947, 1950; Balech, 1944, 1949, 1951;

Rampi, 1950;

Chatton, 1952); locomotion (Peters, 1929). The Dinoflagellata are subdivided into three major groups:
Suborder 1 Prorocentrinea Bivalve shell without furrows Naked or with shell showing furrows. .Suborder 2 Peridiniinea (p. 313) Naked; without furrows; no transverse flagellum Suborder 3 Cystoflagellata (p. 329)

Suborder

Prorocentrinea Poche

Test bivalve; without any groove; with yellow chromatophores; 2 flagella anterior, one directed anteriorly, the other vibrates in a
circle; fresh

or salt water.

Family Prorocentridae Kofoid

Genus Prorocentrum Ehrenberg. Elongate

small, yellowish

oval;

anterior

end

bluntly pointed, with a spinous projection at pole; chromatophores

brown;

salt water. Species (Schiller, 1918, 1928).

a). 36-52/x long;

P. micans E. (Fig. 126,

a cause of "red water."

P. triangulatum Martin. Triangular with rounded posterior end; shell-valves flattened; one valve with a delicate tooth; surface covered with minute pores; margin striated; chromatophores yellowbrown, irregular, broken up in small masses; 17-22^. Martin (1929)

found

it extremely abundant in brackish water in New Jersey. Genus Exuviaella Cienkowski. Subspherical or oval; no anterior

projection, except 2 flagella; 2 lateral chromatophores, large, brown,

each with a pyrenoid and a starch body; nucleus posterior;

salt

and fresh water. Several species (Schiller, 1918, 1928). E. marina C. (Fig. 126, b, c). 36-50 M long. E. apora Schiller. Compressed, oval; striae on margin of valves; chromatophores numerous yellow-brown, irregular in form; 30-32/x (Lebour; Martin); common by 21-26/x (Schiller); 17-22 M by 14-1

in brackish water,

New

Jersey.

E. compressa (Stein). Flattened ellipsoid test; anterior end with a

DINOFLAGELLATA

313

depression through which two flagella emerge; two chromatophores

pale or deep green, each with a pyrenoid; nucleus posterior; no

stigma; 22-26/x by 15-18/z by 11-12/*; fresh and salt water (Thompson, 1950).

Suborder 2 Peridiniinea Poche

Typical dinoflagellates with one to many transverse annuli and a sulcus; 2 flagella, one of which undergoes a typical undulating movement, while the other usually directed posteriorly. According

Fig. 126.

a,

marina,
h,

X420

(Schiitt); d,

Prorocentrum micans, X420 (Schiitt); b, c, Exuviaella e, Cystodinium steini, X370 (Klebs); f, Gleno(Schilling); g, G. pulvisculum,
i,

dinium cinctum, X590

G.

uliginosum, X590 (Schilling); G. neglectum, X650 (Schilling).

to

G.

edax,

X420 (Schilling); X490 (Schilling); j,

Kofoid and Swezy, this suborder

shell

is

divided into two tribes.

Body naked or covered by a thin Body covered by a thick shell

Tribe
1

Tribe 1 Gymnodinioidae Tribe 2 Peridinioidae (p. 324)

Gymnodinioidae Poche
single piece cellulose

Naked or covered by a

membrane with

an-

nulus and sulcus, and 2 flagella; chromatophores abundant, yellow

or greenish platelets or bands; stigma sometimes present; asexual
reproduction, binary or multiple division; holophytic, ho lo zoic, or

314

PROTOZOOLOGY

sap ro zoic; the majority are deep-sea forms; a few coastal or fresh

water forms also occur.

With a cellulose membrane Without shell Furrows rudimentary Annulus and sulcus distinct
Solitary

Family

Cystodiniidae

Family 2 Pronoctilucidae

With ocellus Without ocellus With tentacles Without tentacles

Free-living
Parasitic

Family 3 Pouchetiidae Family 4 Noctilucidae

Family 5 Gymnodiniidae Family 6 Blastodiniidae Family 7 Polykrikidae

(p.

316) 316) 318) 321) 324)

(p.

(p. (p. (p.

Permanently colonial

Family

Cystodiniidae Kofoid and Swezy

Genus Cystodinium Klebs. In swimming phase, oval, with extremely delicate envelope; annulus somewhat acyclic; cyst-membrane drawn out into 2 horns. Species (Pascher, 1928; Thompson,
1949).
C. steini

K.

(Fig. 126, d, e).

Stigma beneath sulcus; chromato-

phores brown; swarmer about 45^ long; freshwater ponds. Genus Glenodinium Ehrenberg. (Glenodiniopsis, Stasziecella Woloszynska). Spherical; ellipsoidal or reniform in end-view; annulus a
circle; several discoidal,

yellow to brown chromatophores;

horseshoe- or rod-shaped stigma in some; often with gelatinous envelope; fresh water.

Many

species

(Thompson, 1950).

G. cinctum E. (Fig. 126,/). Spherical to ovoid; annulus equatorial;

stigma horseshoe-shaped; 43 ai by

40/x.

Morphology and reproduction

stigma; 38/x by
30ju.

(Lindemann, 1929).
G. pulvisculum Stein (Fig. 126, g).

No

G. uliginosum Schilling (Fig. 126, h). 36-48m G. edax S. (Fig. 126, i). 34/x by 33/x.
G. neglectum S. (Fig. 126, j).

by 3G>

30-32 M by 29 M

Family 2 Pronoctilucidae Lebour

Genus Pronoctiluca Fabre-Domergue. Body with an anteroventral tentacle and sulcus; annulus poorly marked; salt water. P. tentaculatum (Kofoid and Swezy) (Fig. 127, a). About 54ju long;
off California coast.

Genus Oxyrrhis Dujardin. Subovoidal, asymmetrical posteriorly; annulus incomplete; salt water. 0. marina D. (Fig. 127, 6). 10-37/x long. Division (Dunkerly, 1921;
Hall, 1925).

DINOFLAGELLATA

315

127. a, Pronoctiluca tentaculatum, X730 (Kofoid and Swezy); Oxyrrhis marina, X840 (Senn); c. Pouchetia fusus, X340 (Schiitt); d, P. maxima, X330 (Kofoid and Swezy); e, Protopsis ochrea, X340 (Wright); f, Nematodinium partitum, X560 (Kofoid and Swezy); g, Proterythropsis crassicaudata, X740 (Kofoid and Swezy); h, Erythropsis cornuta, X340 (Kofoid and Swezy); i, j Noctiluca scintillans (i, side view; j, budding process), X140 (Robin).

Fig.

b,

316

PROTOZOOLOGY
Family 3 Pouchetiidae Kofoid and Swezy

melanosome (pigment mass); sulcus and annulus somewhat twisted; pusules usually present; cytoplasm
Ocellus consists of lens and
colored; salt water (pelagic).

Genus Pouchetia Schutt. Nucleus anterior

central core; lens hyaline;

to ocellus; ocellus

with

red or black pigment mass with a red, brown, yellow, or colorless

body surface usually smooth; ho lo zoic;

en^ystment common;
P. fusus

salt water.

Many
94/t

species (Schiller, 1928a).

41/x; ocellus

About P. maxima Kofoid and Swezy

S. (Fig. 127, c).
20/x; off

by

27m long.

(Fig. 127, d). 145/t

by

92/*; ocellus

California coast.

Genus Protopsis Kofoid and Swezy. Annulus and sulcus similar Gymnodinium or Gyrodinium; with a simple or compound ocellus; no tentacles; body not twisted; salt water. A few species. P. ochrea (Wright) (Fig. 127, e). 55/i by 45/z; ocellus 22/i long;
to those of

Nova

Scotia.

Genus Nematodinium Kofoid and Swezy. With nematocysts; girdle more than 1 turn; ocellus distributed or concentrated, posterior; holozoic; salt water.

N. partitum K. and S. (Fig. 127, /). 91/* long; off California coast. Genus Proterythropsis Kofoid and Swezy. Annulus median; ocellus posterior; a stout

rudimentary tentacle;

salt water.

One

species.

P. crassicaudata K. and S. (Fig. 127, g). 70/t long; off California. Genus Erythropsis Hertwig. Epicone flattened, less than 1/4

hypocone; ocellus very large, composed of one or several hyaline lenses attached to or imbedded in a red, brownish or black pigment body with a red, brown or yellow core, located at left of sulcus; sulcus expands posteriorly into ventro -posterior tentacle; salt water.
Several species.

E. cornuta (Schutt) (Fig. 127,

h). 104/x

long; off California coast

(Kofoid and Swezy).

Family 4 Noctilucidae Kent

Contractile tentacle arises from sulcal area and extends posteriorly;

a flagellum; this group has formerly been included in the

Cystoflagellata; studies

by recent

investigators,
;

particularly
;

by

Kofoid, show its affinity with the present suborder holozoic saltwater.

Genus Noctiluca Suriray. Spherical, bilaterally symmetrical; peristome marks the median line of body; cytostome at the bottom of peristome; with a conspicuous tentacle and a short flagellum; cytoplasm greatly vacuolated, and cytoplasmic strands connect the central mass with periphery; specific gravity is less than that of sea wa-

DINOFLAGELLATA
ter,

31'

due to the presence of an osmotically active substance with a lower specific gravity than sodium chloride, which appears to be
chloride (Goethard and Heinsius); certain granules are luminescent (Fig. 128); cytoplasm colorless or blue-green; sometimes tinged with yellow coloration in center; swarmers formed by budding,

ammonium

and each possesses one

flagellum, annulus,

and

tentale; widely

distributed in salt water; holozoic.

One

species.

N. scintillans f Macartney) (N. miliaris S.) (Figs. 127, i,j; 128). Usually 500-IOOOm in diameter, with extremes of 200/u and 3 mm. Gross (1934) observed that complete fusion of two swarmers (isogametes) results in cyst formation from which trophozoites develop. Acid content of the body fluid is said to be about pH 3. Nuclear di-

as seen under darkfield microscope an active individual; b, a so-called "resting stage," with fat droplets in the central cytoplasm, prior to either division or swarmer
(Pratje). a,

Fig.

128. Noctiluca scintillans,

formation; c, d, appearance of luminescent individuals (F, fat-droplets; K, nucleus; P, peristome; T, tentacle; V, food body; Z, central protoplasm).

318
vision (Calkins, 1898);

PROTOZOOLOGY
morphology and physiology (Goor, 1918;

Kofoid, 1920; Pratje, 1921); feeding (Hofker, 1930); luminescence

(Harvey, 1952).
to

Genus Pavillardia Kofoid and Swezy. Annulus and sulcus similar those of Gymnodinium; longitudinal flagellum absent; stout
mobile tentacle directed posteriorly; salt water. One

finger-like

species.

P. tentaculifera K. and S. 58m

by

27/x;

pale yellow; off California.

Family 5 Gymnodiniidae Kofoid

Naked forms with simple but distinct 1/2-4 turns of annulus; with or without chromatophores; fresh or salt water.
Genus Gymnodinium
laterally

Stein.

Pellicle

delicate;

subcircular;

bi-

symmetrical;

numerous discoid chromatophores

vari-

colored (yellow to deep brown, green, or blue) or sometimes absent;

stigma present in few;

brackish, or fresh water.

many

with mucilaginous envelope;

species (Schiller, 1928a)
;

salt,

Numerous

culti-

vation and development (Lindemann, 1929).

13-25/x

Green chromatophores; 20-32/x by (Thompson, 1950) ponds and lakes. G. rotundatum Klebs (Fig. 129, b). 32-35/x by 22-25 M fresh water.
G. aeruginosum S. (Fig. 129, a).
;

G. palustre Schilling (Fig. 129,

c). 45/z

G. agile Kofoid and Swezy sandy beaches.

(Fig.

by 38^; fresh water. 129, d). About 28m long; along

Genus Hemidinium Stein. Asymmetrical; oval; annulus about on left half. One species. H. nasutum S. (Fig. 129, e). Sulcus posterior; chromatophores yellow to brown; with a reddish brown oil drop; nucleus posterior; transverse fission; 24-28ju by 16-17/x; fresh water. Genus Amphidinium Claparede and Lachmann. Form variable; epicone small; annulus anterior; sulcus straight on hypo cone or also on part of epicone; with or without chromatophores; mainly holophytic, some holozoic; coastal or fresh water. Numerous species
half a turn, only
Schiller, 1928a).

A. lacustre Stein (Fig. 129,

water.

/). 30/t

by

18/x; in

fresh

and

salt (?)

A. scissum Kofoid and Swezy sandy beaches.

in cross-section; epicone

(Fig. 129, g).

50-60m long; along

A. fusiforme Martin. Fusiform, twice as long as broad: circular rounded conical; annulus anterior; hypocone 2-2.5 times as long as epicone; sulcus obscure; body filled with

DINOFLAGELLATA

319

Fig. 129. a, Gymnodinium aeruginosum, X500 (Schilling); b, G. rotundatum, X360 (Klebs); c, G. palustre, X360 (Schilling); d, G. agile, X740 (Kofoid and Swezy); e, Hemidinium nasutum, X670 (Stein); f, Amphidinium lacustre, X440 (Stein); g, A. scissum, X8S0 (Kofoid and Swezy); h, Gyrodinium biconicum, X340 (Kofoid and Swezy); i, G. hyalinum, X670 (Kofoid and Swezy); j, Cochlodinium atromaculatum, X340 (Kofoid and Swezy); k, Torodinium robustum, X670 (Kofoid and Swezy); 1, Massartia nieuportensis, X670 (Conrad); m, Chilodinium cruciatum, X900 (Conrad); n, o, Trochodinium prismaticum, X1270 (Conrad); p, Ceratodinium asymmetricum, X670 (Conrad).

320

PROTOZOOLOGY
;

yellowish green chromatophores except at posterior end stigma dull

orange, below girdle; nucleus ellipsoid, posterior to annulus; pellicle delicate; 17-22ju by 8-1 1/z in diameter. Martin (1929) found that it

was extremely abundant

in parts of

Delaware Bay and gave

rise to

red coloration of the water ("Red water").

Genus Gyrodinium Kofoid and Swezy. Annulus descending left extending from end to end; nucleus central; pusules; surface smooth or striated; chromatophores rarely present; cytoplasm colored; holozoic; salt or fresh water. Many species (Schiller,
spiral; sulcus

1928a).
Q. biconicum K.
fornia.
i). About 24^ long; fresh water. Twisted at least 1.5 turns; annulus descending left spiral; pusules; cytoplasm colorless to highly colored; chromatophores rarely present; holozoic; surface smooth or striated;

and

S. (Fig. 129, h).

68 n long; salt water;

off Cali-

G. hyalinum (Schilling) (Fig. 129,

Genus Cochlodinium

Schlitt.

salt water.

Numerous

species (Schiller, 1928a).

C. atromaculatum Kofoid
72ju;

and Swezy

(Fig. 129, j). 183-185/x

by

longitudinal flagellum 45/x long; off California.

several

Genus Torodinium Kofoid and Swezy. Elongate; epicone

shaped cone; sulcus long; nucleus greatly elongate;
species (Schiller, 1928).

times longer than hypocone; annulus and hypocone form augursalt water. 2

T. robustum K. and S. (Fig. 129, k). 67-75/z long; off California. Genus Massartia Conrad. Cylindrical; epicone larger (9-10 times longer and 3 times wider) than hypocone; no sulcus; with or without yellowish discoid chromatophore (Thompson, 1950).

nieuportensis C. (Fig. 129,

1).

28-37/x long; brackish water.

Genus Chilodinium Conrad.

Ellipsoid;

posterior end

broadly

rounded, anterior end narrowed and drawn out into a digitform process closely adhering to body; sulcus, apex to 1/5 from posterior
end; annulus oblique, in anterior 1/3 (Conrad, 1926). C. cruciatum C. (Fig. 129, m). 40-50ju by 30-40/z; with trichocysts;
brackish water.

Genus Trochodinium Conrad. Somewhat similar to Amphidinium; epicone small, button-like; hypocone with 4 longitudinal rounded ridges; stigma; without chromatophores.
T. prismaticum C. (Fig. 129, n, o).
18-22/x

by

9-12;u;

epicone

5-7

jit

in

diameter; brackish water (Conrad, 1926).

Genus Ceratodinium Conrad. Cuneiform; asymmetrical, colormore or less flattened; annulus complete, oblique; sulcus on half of epicone and full length of hypocone; stigma.
less,

DINOFLAGELLATA
C.

321
10/x;

asymmetricum C.

(Fig. 129, p).

68-80^ by about

brackish

water (Conrad, 1926).

Family 6 Elastodiniidae Kofoid and Swezy

there occur trophocyte (Chatton)

on plants and animals; in colony forming genera, by which organism is attached to host and more or less numerous gonocytes (Chatton). Taxonomy
All parasitic in or

(Chatton, 1920; Reichenow, 1930).

Genus BJastodinium Chatton. In the gut

of copepods; spindle-

shaped, arched, ends attenuated; envelope (not cellulose) often with

2 spiral rows of bristles; young forms binucleate;

when

present,

chromatophores in yellowish brown network; swarmers similar to

those of Gymnodinium; in salt water.

Many species.
235/*

B. spinulosum C. (Fig. 130,

5-10ju; in

a).

About

by

33-39/z;

swarmers

Palacalanus parvus, Clausocalanus arcuicornis and C.

furcatus.

stalk; nucleus large; often

lida,

Genus Oodinium Chatton. Spherical or pyriform; with a short with yellowish pigment; on Salpa, AnneSiphonophora, marine
fishes, etc.

0. poucheti

(Lemmermann)

(Fig. 130,

duals

up

to 170/x long; bright yellow ochre;

detached and free, dividing swarmers; on the tunicate. Oikopleura dioica.

O. ocellatum
fish

Fully grown indivimature forms become into numerous gymnodinium-like

b,

c).

Brown (Fig. 131, a, b). Attached to the gill filaments of by means of cytoplasmic processes; oval in form; 12m by 10m to 104m by 80m, average 60m by 50m; nucleus spherical; many chromatophores and starch grains; a stigma. When grown, the organism drops off the gill and becomes enlarged to as much as 150m in diameter. Soon the cytoplasmic processes and the broad flagellum are retracted and the aperture of shell closes by secretion of cellulose substance. The body divides up to 128 cells, which become flagellated and each divides once more. These flagellates, 12/x by 8m, reach the gills of fish and become attached (Brown, 1931; Nigrelli,
marine
1936).
c, d). Pyriform; 12ju by 7.5m to green chromatophores variable in size and shape; no stigma; without flagella; filopodia straight or branched; the or-

O. limneticum Jacobs (Fig. 131,

20ju

by

13/x; light

ganism grows into about 60m long in three days at 25C; observed maximum, 96m by 80m; starch becomes abundant; fission takes place in cyst; flagellate forms measure about 15m long; ectoparasitic on the integument of freshwater fishes in aquaria (Jacobs, 1946).

322

PROTOZOOLOGY
elongate, spherical

Genus Apodinium Chatton. Young individuals

or pyriform; binucleate; adult colorless; formation of numerous

swarmers in adult stage is peculiar in that lower of the 2 individuals formed at each division secretes a new envelope, and delays its

nium
(d,
f,

Fig. 130. a, Blastodinium spinxdosum, X240 (Chatton); b, c, Oodipoucheti (c, a swarmer) (Chatton); d, e, Apodinium mycetoides

swarmer-formation, X450; e, a younger stage, X640) (Chatton); Chytriodiniuxn parasiticum in a copepod egg (Dogiel); g, Trypanodinium ovicola, X1070 (Chatton); h, Duboscqella tintinnicola (Duboscq and Collin); i, j, Haplozoon clymenellae (i, mature colony, X300; j, a swarmer,

X1340) (Shumway);

k,

Syndinium

turbo,

X1340 (Chatton);

1,

Paradi-

nium

Ellobiopsis chattoni on Calanus finmarchicus (Caullery); n, Paraellobiopsis coutieri (Collin).

poucheti,

X800 (Chatton); m,

DINOFLAGELLATA
leaving several open cups; on tunicates.

323

further division until the upper one has divided for the second time,

A. mycetoides C. (Fig. 130,

lucida.

d, e).

On

gill-slits

of Fritillaria pel-

Genus Chytriodinium Chatton. In eggs of planktonic copepods; young individuals grow at the expense of host egg and when fully formed, body divides into many parts, each producing 4 swarmers.
Several species.
C. parasiticum (Dogiel) (Fig. 130, /). In

copepod eggs; Naples.

Genus Trypanodinium Chatton. In copepod eggs; swarmer-stage only known.

Fig.

131. a,

Oodinium

ocellatum,

b, a free living flagellate form,

X760

(Nigrelli);

recently detached from host gill; c, d, 0. limneticum, X800

(Jacobs).

T. ovicola C. (Fig. 130, g). Swarmers biflagellate; about 15ju long. Genus Duboscqella Chatton. Rounded cell with a large nucleus; parasitic in Tintinnidae. One species. D. tiniinnicola (Lohmann) (Fig. 130, h). Intracellular stage oval,

about 100^ in diameter with a large nucleus; swarmers biflagellate. Genus Haplozoon Dogiel. In gut of polychaetes; mature forms composed of variable number of cells arranged in line or in pyramid;
salt water.

Many

species.

H. clymenellae (Calkins) (Microtaeniella clymenellae

i,j).

C.) (Fig. 130,

In the intestine of Clymenella torquata; colonial forms consist of

of marine

250 or more

cells; Woods Hole (Shumway, 1924). Genus Syndinium Chatton. In gut and body cavity

copepods; multinucleate round cysts in gut considered as young

324

PROTOZOOLOGY

forms; multinucleate body in host body cavity with numerous

needle-like inclusions.

Paracalanus parvus, Corycaeus venCalanus finmarchicus; swarmers about 15/x long. Genus Paradinium Chatton. In body-cavity of copepods; multinucleate body without inclusions; swarmers formed outside the host body. P. poucheti C. (Fig. 130, 1). In the copepod, Acartia clausi; swarmers about 25,u long, amoeboid. Genus Ellobiopsis Caullery. Pyriform; with stalk; often a septum near stalked end; attached to anterior appendages of marine copeS. turbo C. (Fig. 130, k). In
ustus,

pods.
E. chattoni C. (Fig. 130, m).

Up

to 700/c long;

on antennae and

oral appendages of Calanus finmarchicus, Pseudocalanus elongatus

and Acartia clausi. Development (Steuer, 1928). Genus Paraellobiopsis Collin. Young forms stalkless; mature individuals in chain-form; on Malacostraca.
P. coutieri C. (Fig. 130, n).

spherical;

On appendages

of Nebalia bipes.

Family

7 Polykrikidae

Kofoid and Swezey

Two,

4,

8,

or 16 individuals permanently joined; individuals

entire

similar to

Gymnodinium; sulcus however extending

body

length; with nematocysts (Fig.

132, 6); greenish to pink; nuclei

salt water.

about 1/2 the number of individuals; holozoic;

cysts (Hovasse, 1951).

Nemato-

Genus Polykrikos

Btitschli.

With the above-mentioned characters;

salt or brackish water. Species (Schiller, 1928).

P. kofoidi (Chatton) (Fig. 132, a, 6). Greenish grey to rose; composed of 2, 4, 8, or 16 individuals; with nematocysts; each nematocyst possesses presumably a hollow thread, and discharges under suitable stimulation its content; a binucleate colony composed of 4
individuals about 110m long; off California. P. barnegatensis Martin. Ovate, nearly circular in cross-section,

concave ventrally; composed of 2 individuals; constriction beaded nucleus in center; annuli descending left spiral, displaced twice their width; sulcus ends near anterior end; cytoplasm colorless, with numerous oval, yellow-brown chromatophores; nematocysts absent; 46m by 31.5/*; in brackish water of Barnegat Bay.
slightly
slight;

Tribe 2 Peridinioidae Poche

The

shell

composed of epitheca, annulus and hypotheca, which

may be

divided into numerous plates; body form variable.

DINOFLAGELLATA
. .

325

With annulus and sulcus Shell composed of plates; but no suture. Family 1 Peridiniidae (p. 326) Breast plate divided by sagittal suture. Family 2 Dinophysidae (p. 328) Without annulus or sulcus Family 3 Phytodiniidae (p. 329)

b,

a, b, Polykrikos kofoidi (a, colony of four individuals, X340; a nematocyst, X1040) (Kofoid and Swezy); c, Peridinium tabulatum, X460 (Schilling); d, P. divergens, X340 (Calkins); e, Ceratium hirundi-

Fig. 132.

nella,

X540

(Stein);

f.

C. longipes,

X100
i,

(Wailes);

g,

C. tripos,

(Wailes); h, C. fusxis,

X100

(Wailes);

Heterodinium scrippsi,

X140 X570

(Kofoid and Adamson).

326

PROTOZOOLOGY
Family
1

Peridiniidae

Kent

Shell

composed of numerous

plates; annulus usually at equator,

and vary in shape and number among different species; in many species certain plates drawn out into various processes, varying greatly in different seasons and localities even among one and the same species; these processes seem to retard descending movement of organisms from upper to lower level in water when flagellar activity ceases; chromatophores numerous small platelets, yellow or green; some deep-sea forms without chromatophores; chain formation in some forms; mostly surface and pelagic inhabitants in
covered by a plate
as cingulum; variously sculptured
finely perforated plates

known

fresh or salt water.

Genus Peridinium Ehrenberg. Subspherical

often with short horns and epitheca

to ovoid; reniform in

cross-section; annulus slightly spiral with projecting rims;

hypotheca

drawn out;

colorless, green, or

brown; stigma usually present; cysts spherical; salt or fresh water. Numerous species. Species and variation (Bohm, 1933; Diwald, 1939); Chromatophore and pyrenoid (Geitler, 1926). P. tabulation Claparede and Lachmann (Fig. 132, c). 48/t by 44/i;
fresh water.

P. diver gens (E.) (Fig. 132,

salt water.

d).

About

45/i in

diameter; yellowish,

Genus Ceratium Schrank. Body flattened; with one anterior and 1-4 posterior horn-like processes; often large; chromatophores yellow, brown, or greenish; color variation conspicuous; fission
to take place at night
is

said

and

in the early

Numerous

species; specific

morning; fresh or salt water. identification is difficult due to a great

variation (p. 223). Biology and morphology (Entz, 1927); encyst-

ment (Entz,
ical

1925).
e). 1

C. hirundinella (Muller) (Figs. 94; 132,

apical

and 2-3 antap223); chain-

horns; seasonal and geographical variations

(p.

formation frequent; 95-700/x long; fresh and salt water. Numerous varieties. Reproduction (Entz, 1921, 1931; Hall, 1925a; Borgert,
1935); holozoic nutrition (Hofeneder, 1930).
C. longipes (Bailey) (Fig. 132, /).

About

210/i

by 51-57 M

salt

water.
C. tripos (Muller) (Fig. 132,0).

About 225/i by 75/x; salt water. Wailes

(1928) observed var. atlantica in British Columbia; Martin (1929)

Barnegat Inlet, New Jersey. Nuclear division (Schneider, 1924). C.fusus (Ehrenberg) (Fig. 132, h). 300-600/x by 15-30/*; salt water; widely distributed; British Columbia (Wailes), New Jersey (Martin),
in
etc.

DINOFLAGELLATA
Genus Heterodinium Kofoid. Flattened or spheroidal; 2
short, narrow; shell hyaline, reticulate, porulate; salt water.

327
large

antapical horns; annulus submedian; with post-cingular ridge; sulcus

Numer-

ous species.

H. scrippsi K.
(tropical).

(Fig. 132,

i).

130-155/x long; Pacific and Atlantic

Genus Dolichodinium Kofoid and Adamson. Subcorneal, elongate; without apical or antapical horns; sulcus only 1/2 the length of hypotheca; plate porulate; salt water. D. lineatum (Kofoid and Michener) (Fig. 133,
tropical Pacific.
a). 58/z long;

eastern

Genus Goniodoma

Stein. Polyhedral

with a deep annulus; episize,

theca and hypotheca slightly unequal in

fresh or salt water.

composed

of regularly

arranged armored plates; chromatophores small brown platelets;

About 50> long; salt water. Genus Gonyaulax Diesing. Spherical, polyhedral, fusiform, elongated with stout apical and antapical prolongations, or dorsoG. acuminata (Ehrenberg) (Fig. 133, b).

ventrally flattened; apex never sharply attenuated; annulus equatorial; sulcus

from apex to antapex, broadened posteriorly; plates 1-6 apical, 0-3 anterior intercalaries, 6 precingulars, 6 annular

plates, 6 postincingulars, 1 posterior intercalary

and

antapical;

porulate; chromatophores yellow to dark brown, often dense; with-

out stigma; fresh, brackish or salt water. 1911; Whedon and Kofoid, 1936).
G. polyedra Stein (Fig. 133,
c).

Numerous

species (Kofoid,

Angular, polyhedral; ridges along

sutures, annulus displaced 1-2 annulus widths, regularly pitted; salt

water. "Very abundant in the San Diego region in the

summer

plankton, July-September,
water,'

when

it

causes local outbreaks of 'red

which extend along the coast of southern and lower Cali-

fornia" (Kofoid, 1911; Allen, 1946).

The organisms occurred

also in

water off the beach of Areia Branca, Portugal, and caused "red water" during the day and an extreme luminescence when agitated at night (Santosof plankton) in pools of sea

abundance (85 per cent

Pinto, 1949).
G. apiculata (Penard) (Fig. 133, d). Ovate, chromatophores yel-

lowish brown; 30-60/x long; fresh water.

Genus Spiraulax Kofoid. Biconical; apices pointed; sulcus not

reaching
water.
S. jolliffei

apex;

no

ventral

pore;

surface

heavily

pitted;

salt

(Murray and Whitting)

(Fig.

133, e).

132^ by 92^;

California (Kofoid, 1911a).

32*

PROTOZOOLOGY
(1950).

Genus Woloszynskia Thompson

ate form between Gymnodinioidae

An

apparently intermedi-

and Peridinioidae.

Family 2 Dinophysidae Kofoid

Genus Dinophysis Ehrenberg. Highly compressed; annulus widened, funnel-like, surrounding small epitheca; chromatophores yel-

low; salt water. Several species (Schiller, 1928). Morphology and

taxonomy (Tai and Skogsberg,

1934).

Fig. 133.
b,

a,

Dolichodinium lineatum,
(Stein);

Goniodoma acuminata, X340

d,

X670 (Kofoid and Adamson), c, Gonyaulax polyedra, X670

;

right side of theca, X340 (Kofoid); X780 g, h, Oxyphysis oxytoxoides,

e, Spiraulax jolliffei, Dinophysis acuta, X580 (Schutt); (Kofoid); i, Phytodinium simplex, X340 (Klebs); j, k, Dissodinium lunula: j, primary cyst (Dogiel); k, secondary cyst with 4 swarmers (Wailes), X220.

(Kofoid);

G.

apiculata,

X670 (Lindemann)
f,

DINOFLAGELLATA

329

D. acuta E. (Fig. 133,/). Oval; attenuated posteriorly ;54-94/z long; widely distributed; British Columbia (Wailes). Genus Oxyphysis Kofoid. Epitheca developed; sulcus short; sulcal
lists

feebly developed; sagittal suture conspicuous; annulus im-

pressed; salt water (Kofoid, 1926).

0. oxytoxoides K. (Fig. 133,
g, h).

63-68 M by

15/*; off

Alaska.

Family 3 Phytodiniidae Klebs

Genus Phytodinium Klebs. Spherical or

P. simplex K. (Fig. 133,
fresh water.
i).

ellipsoidal;

without fur-

rows; chromatophores discoidal, yellowish brown.

Spherical or oval; 42-50/x

by 30-45m
cyst,

Genus Dissodinium Klebs (Pyrocystis Paulsen). Primary

spherical, uninucleate; contents divide into

ary cysts which become set free; Gymnodinium-like swarmers; salt water.

8-16 crescentic secondin them are formed 2, 4, 6, or 8

Fig. 134.

a,

Leptodiscus medusoides,
pileolus,

X50 (Hertwig);
(Kofoid).
k).

b,

Craspedotella

X110
j,

D. lunula (Schutt) (Fig. 133,

distributed; British

Primary cysts 80-155/*

22/x long;

in

diameter; secondary cysts 104-130/z long; swarmers

widely

Columbia (Wailes).

Suborder 3 Cystoflagellata Haeckel

Since Noctiluca which had for many years been placed in this suborder, has been removed, according to Kofoid, to the second suborder, the Cystoflagellata becomes a highly ill-defined group and
includes two peculiar marine forms: Leptodiscus medusoides Hertwig
(Fig. 134, a),

of which are

and Craspedotella pileolus Kofoid medusoid in general body form.

References

(Fig. 134, b),

both

Allen, W. E.: (1946) Significance

news, 24:49.

of "red

water"

in the sea.

Turtox

Balech, E.: (1949) Etude de quelques especes de Peridinium, souvent confondues. Hydrobiologia, 1:390. (1951) Deuxieme contribution a la connaissance des Peridinium. Ibid., 3:305.

330

PROTOZOOLOGY

A.: (1933) Beobachtungen an adriatischen Peridinium-Arten. Arch. Protist, 80:303. Borgert, A.: (1935) Fortpflanzungsvorgange und Heteromorphismus bei marinen Ceratien, etc. Ibid., 86:318. Brown, E. M.: (1931) Note on a new species of dinoflagellate from the gills and epidermis of marine fishes. Proc. Zool. Soc. London,

Bohm,

1:345.

Calkins, G. N.: (1898) Mitosis in Noctiluca milliaris. 58 pp. Chatton, E.: (1920) Les Peridiniens parasites: Morphologie,

re-

production, ethologie. Arch. zool. exper. gen., 59:1. (1952) Classe des Dinoflagelles ou Peridiniens. In: Grasse
(1952), p. 310.

Conrad, W.: (1926) Recherches sur

les flagellates de nos eaux saumatres. I. Arch. Protist., 55:63. Diwald, K.: (1939) Ein Beitrag zur Variabilitat und Systematik der Gattung Peridinium. Ibid., 93:121. Dunkerly, J. S.: (1921) Nuclear division in the dinoflagellate, Oxyrrhis marina. Proc. Roy. Phys. Soc, Edinburgh, 20:217. Eddy, S.: (1930) The freshwater armored or thecate dinoflagellates. Tr. Am. Micr. Soc, 49:1. Entz, G.: (1921) Ueber die mitotische Teilung von Ceratium hirundinella. Arch. Protist., 43:415. (1925) Ueber Cysten und Encystierung der SiisswasserCeratien. Ibid., 51:131. (1927) Beitrage zur Kenntnis der Peridineen. Ibid., 58:344. (1931) Analyse des Wachstums und Teilung einer Population sowie eines Individuums des Protisten Ceratium, etc. Ibid., 74:

310.

Fritsch, F. E.: (1935) The structure and reproduction

Galtsoff, P.

S.: (1948)

Red

tide: etc. Spec.

Sc

of the algae. Rep., U. S. Fish

Wildl. Service, no. 46. (1949) The mystery of the red tide. Sc. Monthly, 68:109. Geitler, L.: (1926) Ueber Chromatophoren und Pyrenoide bei Peridineen. Arch. Protist., 53:343. Goor, A. C. J. Van: (1918) Die Cytologie von Noctiluca miliaris.
Ibid.,

39:147.
(1943)

Graham, H. W.:

Gymnodinium catenatum,

etc.

Tr.

Am.

Micr. Soc, 62:259.

Gross, F.: (1934) Zur Biologie und Entwicklungsgeschichte von

Hall, R.

Noctiluca miliaris. Arch. Protist., 83:178. P.: (1925) Binary fission in Oxyrrhis marina. Univ. California Publ. Zool, 26:281. (1925a) Mitosis in Ceratium hirundinella, etc. Ibid, 28:29. Harvey, E. N.: (1952) Bioluminescence. New York. Hofeneder, H. (1930) Ueber die animalische Ernahrung von Ceratium, etc. Arch. Protist, 71:1. Hofker, J.: (1930) Ueber Noctiluca scintillans. Ibid, 71:57. Hovasse, R.: (1951) Contribution a l'etude de la cnidogenese chez les Peridiniens. I. Arch. zool. exper. gen, 87:299. new parasitic dinoflagellate from freshwater Jacobs, D. L.: (1946) fish. Tr. Am. Micr. Soc, 65:1.
:

DINOFLAGELLATA
Ketchum,
17.

331

B. H. and Keen, Jean: (1948) Unusual phosphorus concentrations in the Florida "red tide" sea water. J. Mar. Res., 7:
of

Kofoid, C. A.: (1907) The plate

Ceratium,

etc. Zool.

Anz., 32:

177. (1909) On Peridinium steinii, etc. Arch. Protist., 14:25. (1911) Dinoflagellata of the San Diego Region. IV. Uni. Cal. Publ. Zool., 8:187.

(1911a) V. Ibid., 8:295. new morphological interpretation of Noctiluca, etc. (1920) Ibid., 19:317. (1926) On Oxyphysis oxytoxoides, etc. Ibid., 28:203. (1931) Report of the biological survey of Mutsu Bay. XVIII. Sc. Rep. Tohoku Imp. Uni., Biol., 6:1. and Adamson, A. M.: (1933) The Dinoflagellata: the family Heterodiniidae, etc. Mem. Mus. Comp. Zool. Harvard, 54:1. and Swezy, Olive: (1921) The free-living unarmored Dinoflagellata. Mem. Univ. California, 5:1. Lebour, Marie V. (1925) The dinoflagellates of northern seas.

London.

Lindemann,

E.: (1929) Experimentelle Studien uber die Fortpflanzungserscheinungen der Siisswasserperidineen auf Grund von Reinkulturen. Arch. Protist., 68:1. Martin, G. W.: (1929) Dinoflagellates from marine and brackish waters of New Jersey. Univ. Iowa Stud. Nat. Hist., 12, no. 9. Nigrelli, R. F.: (1936) The morphology, cytology and life-history
of Oodinium ocellatum Brown, etc. Zoologica, 21 129. Pascher, A.: (1928) Von einer neue Dinococcale, etc. Arch.
:

Protist.,

63:241. Peters, N.: (1929) Ueber Orts- und Geisselbewegung bei marinen Dinoflagellaten. Ibid., 67:291. Playfair, G. I.: (1919) Peridineae of New South Wales. Proc. Linn. Soc. N.S.Wales, 44:793. Pratje, A.: (1921) Noctiluca miliaris Suriray. Beitrage zur Morphologie, Physiologie und Cytologic I. Arch. Protist., 42:1. Prescott, G. W. (1928) The motile algae of Iowa. Univ. Iowa Stud. Nat. Hist., 12:5. Rampi, L. (1950) Peridiniens rares ou nouveaux pour la Pacifique Sud-Equatorial. Bull. lTnst. Oceanogr., no. 974. Reichenow, E.: (1930) Parasitische Peridinea. In: Grimpe's Die Tierwelt der Nord- und Ost-See. Pt. 19, II, d3. Santos-Pinto, J. d.: (1949) caso de "red water" motivado por abundancia anormal de Gonyaulax poliedra. Bol. Soc. Port. Ci. Nat., 17:94. Schiller, J.: (1918) Ueber neue Prorocentrum- und ExuviellaArten, etc. Arch. Protist., 38:250. (1928) Die planktischen Vegetationen des adriatischen Meers. I. Ibid., 61:45. (1928a) II. Ibid., 62:119. Schilling, A.: (1913) Dinoflagellatae (Peridineae). Die Slisswasserflora Deutscblands. Pt. 3.
: :

Um

332

PROTOZOOLOGY
bei

Schneider, H.: (1924) Kern und Kernteilung

Arch. Protist., 48:302.

Ceratium

tripos.

Shumway, W.:
59.

(1924)

The genus Haplozoon,

etc. Jour. Parasit., 11 etc.

Steuer, A.: (1928) Ueber Ellobiopsis chattoni Caullery,

Protist., 60:501.

Arch.

Tai, L.-S. and Skogsberg, T.: (1934) Studies on the Dinophysoidae, etc. Ibid., 82:380. Thompson, R. H.: (1947) Freshwater dinoflagellates of Maryland. Chesapeake Biol. Lab. Publ., no. 67. (1949) Immobile Dinophyceae. I. Am. J. Bot., 36:301. (1950) A new genus and new records of freshwater Pyrrophyta, etc. Lloydia, 13:277. Wailes, G. H.: (1928) Dinoflagellates and Protozoa from British Columbia. Vancouver Mus. Notes, 3. (1934) Freshwater dinoflagellates of North America. Ibid., 7,

Whedon, W.

Suppl., 11. F.

and Kofoid, C. A.: (1936) Dinoflagellates of the San Francisco region. I. Univ. California Publ. Zool., 41:25.

Chapter

13

Subclass 2 Zoomastigina Doflein

lack chromatophores and body organTHE Zoomastigina vary greatly from a simple a very complex The
their
izations
to

type.

majority possess a single nucleus which is, as a rule, vesicular in structure. Characteristic organellae such as parabasal body, axostyle, etc., are present in numerous forms and myonemes are found
ual reproduction

some species. Nutrition is holozoic or saprozoic (parasitic). Asexis by longitudinal fission; sexual reproduction is unknown. Encystment occurs commonly. The Zoomastigina are freein

living or parasitic in various animals.

With pseudopodia besides flagella With flagella only With 1-2 flagella With 3-8 flagella With more than 8 flagella

Order

Rhizomastigina
(p. (p. (p.

Order 2 Protomonadina Order 3 Polymastigina Order 4 Hypermastigina

339) 369) 404)

Order

Rhizomastigina Butschli

between the Sarcodina and the Mastigophora are placed here. Flagella vary in number from one to several and pseudopods also vary greatly in number and in appearof borderline forms

A number

ance.

With many flagella With 1-3 rarely 4 flagella

Family 1 Multiciliidae Family 2 Mastigamoebidae

1

Family

Multiciliidae

Poche

Genus

Multicilia Cienkowski. Generally spheroidal, but amoeboid;

flagella,

with 40-50

long and evenly distributed; one or more nuclei;

holozoic; food obtained

fission; fresh

by means

of pseudopodia; multiplication

by

or salt water.
C. (Fig. 135, a). 20-30ju in diameter; uninucleate; salt

M. marina
water.

M.

lacustris

Lauterborn

(Fig. 135, b). Multinucleate; 30-40/x in

diameter; fresh water.

Family 2 Mastigamoebidae

With 1-3 or rarely 4 flagella and axo podia or lobo podia; uninucleflagellum arises from a basal granule which is connected with the nucleus by a rhizoplast; binary fission in both trophic and encysted stages; sexual reproduction has been reported in one speate;
cies; holozoic

or saprozoic; the majority are free-living, though a few

parasitic.

333

334

PROTOZOOLOGY
Monomastiand endocommensal. Species
Frenzel).

Genus Mastigamoeba Schulze (Mastigina

connected with nucleus; fresh water,
(Klug, 1936).
soil or

gote, uninucleate, with finger-like pseudopodia; flagellum long

M.

aspera

S. (Fig. 135, c).

Subspherical or oval; during locomotion

elongate and narrowed anteriorly, while posterior end rounded or

Fig. 135. a, Multicilia marina, X400 (Cienkowski) b, M. lacustris, X400 (Lauterborn) c, Mastigamoeba aspera, X200 (Schulze); d, M, longifilum, X340 (Stokes); e, M. setosa, X370 (Goldschmidt); f, Masti; ;

gellavitrea,

X 370

(Goldschmidt).

lobed; numerous pseudopods slender, straight; nucleus near flagellate end; 2 contractile vacuoles;

150-200> by about 50>; in ooze of

pond.

M.

longifilum Stokes (Fig. 135, d). Elongate, transparent; flagel-

lum twice body length; pseudopods few, short; contractile vacuole anterior; body 28/i long when extended, contracted about 10>; stagnant water.

ZOOMASTIGINA, RHIZOMASTIGINA
M. M.
frogs
setosa

335

(Goldschmidt) (Fig. 135,

e).

Up

to 140m long.

hylae (Frenzel) (Fig. 136, a). In the hind-gut of the tadpoles of

and toads: 80-135^ by 21-31 m; flagellum about 10m long

(Becker, 1925). Development (Ivanic, 1936).

Genus Mastigella Frenzel. Flagellum apparently not connected with nucleus; pseudopods numerous, digitate; body form changes
actively

M.

vitrea

and continuously; contractile vacuole. Goldschmidt (Fig. 135,/). 150/x long; sexual reproduction
spheroidal, with a single

(Goldschmidt).

Genus Actinomonas Kent. Generally

flagellum and radiating pseudopods; ordinarily attached to foreign

object with a cytoplasmic process, but swims freely

it;

by withdrawing

nucleus central; several contractile vacuoles; ho lo zoic.

10/x in

A. mirabilis K. (Fig. 136, 6). Numerous simple filopodia; about diameter; flagellum 20ju long; fresh water. Genus Dimorpha Gruber. Ovoid or subspherical; with 2 flagella

and radiating axopodia, all arising from an eccentric centriole; nucleus eccentric pseudopods sometimes withdrawn fresh water. Spe;

cies (Pascher, 1925).

D. mutans G. (Fig. 136,

30/x long.

c).

15-20;u in diameter; flagella

about 20-

Genus Tetradimorpha Hsiung. Spherical with radiating axopodia;

four flagella originate in a slightly depressed area; nucleus central.

When disturbed, all axopodia turn away from the flagellated pole and are withdrawn into body, and the organism undergoes swimming movement; freshwater ponds. T. radiata H. (Fig. 136, d, e). Body 27-38m in diameter; axopodia
27-65m long; flagella 38-57/z long (Hsiung, 1927). Genus Pteridomonas Penard. Small, heart-shaped; usually attached with a long cytoplasmic process; from opposite pole there arises a single flagellum, around which occurs a ring of extremely fine filopods; nucleus central; a contractile vacuole; ho lo zoic; fresh water.
P. pulex P. (Fig. 136,/). 6-12ju broad.

Genus Histomonas Tyzzer. Actively amoeboid; mostly rounded, sometimes elongate; a single nucleus; an extremely fine flagellum arises from a blepharoplast, located close to nucleus; axostyle (?) sometimes present; in domestic fowls. One species. H. meleagridis (Smith) {Amoeba meleagridis S.) (Fig. 137). Actively amoeboid organism; usually rounded; 8-21/x (average 10-14/x)
nucleus circular or pyriform with usually a endosome; a fine flagellum; food "vacuoles contain bacteria, starch grains and erythrocytes; binary fission; during division flagelin the largest diameter;

large

336

PROTOZOOLOGY

lum is discarded; cysts unobserved; in young turkeys, chicks, grouse, and quail. Bayon and Bishop (1937) successfully cultured the organism from hen's liver. Morphology of the cultured forms (Bishop,
1938).

This organism is the cause of enterohepatitis known as "blackhead," an infectious disease, in young turkeys and also in other fowls, in which it is often fatal. Smith (1895) discovered the organ-

ism and considered

it

mucosa

of the intestine

an amoeba (1910). It invades and destroys the and caeca as well as the liver tissues. Tropho-

Fig.

136. a,

Dimorpha mutans, X940 (Blochmann); d, e, Tetradimorpha radiata CHsiung) (d, a typical specimen, X430; e, swimming individual, X300); f, Pteridomonas pulex, X540 (Penard); g, Rhizomastix gracilis, X1340 (Mackinnon).
mirabilis,
;

XI 140

Mastigamoeba (Griessmann)

hylae,
c,

X690

(Becker);

b,

Actinomonas

ZOOMASTIGINA, RHIZOMASTIGINA
zoites

337

voided

in faeces

by

infected birds

may become

the source of

in by young birds with drink or food. Tyzzer (1920) found the organism to possess a flagellate stage and established the genus Histomonas for it. Tyzzer and Fabyan (1922) and Tyzzer (1934) demonstrated that the organism is transmissible from bird to bird in the eggs of the nematode Heterakis gallinae, which method appears to be a convenient and reliable one for producing Histomonas infection in turkeys (McKay and Morehouse,

new

infection

when taken

Fig. 137. Histomonas meleagridis. a-d, from host animals (Wenrich); e-h, from cultures (Bishop), a, b, organisms in caecum of chicken (in a Tyzzer slide); c, an individual from pheasant showing "ingestion tube" with a bacterial rod; d, a large individual from the same source, all

X1765;

e,

an amoeboid form;

f,

a rounded form with axostyle

(?); g, h,

stages in nuclear division, X2200.

Desowitz (1950) noticed in a Heterakis two enlarged gut cells with amoebulae which he suggested might be a stage of this protozoan. Niimi (1937) reported that the organism enters through the mouth of the nematode and invades its eggs. Dobell (1940) points out the similarity between this flagellate and Dientamoeba fragilis (p. 462). Wenrich (1943) made a comparative study of forms found in
1948).
filled

338

PROTOZOOLOGY

the caecal smears of wild ring-neck pheasants and of chicks. The organisms measured 5-30^ in diameter and possessed 1-4 flagella, though often there were no flagella. Genus Rhizomastix Alexeieff. Body amoeboid; nucleus central: blepharoplast located between nucleus and posterior end; a long

from it to anterior end and continues into the flagellum; without contractile vacuole; division in spherical cyst. R. gracilis A. (Fig. 136, g). 8-14ju long; flagellum 20/x long; in
fiber runs

intestine of axolotles

and

tipulid larvae.

References
P. and Bishop, Ann: (1937) Cultivation of Histomonas meleagridis from the liver lesions of a hen. Nature, 139:370. Becker, E. R. (1925) The morphology of Mastigina hylae (Frenzel) from the intestine of the tadpole. J. Parasit., 11:213. Bishop, Ann: (1938) Histomonas meleagridis, etc. Parasit., 30:181.

Bayon, H.

S.: (1950) Protozoan hyperparasitism of Heterakis Nature, 165:1023. Dobell, C: (1940) Research on the intestinal Protozoa of monkeys and man. X. Parasit., 32:417. Hsiung, T.-S.: (1927) Tetradimorpha radiata, etc. Tr. Am. Micr. Soc, 46:208. Klug, G.: (1936) Neue oder wenig bekannte Arten der Gattungen Mastigamoeba, etc. Arch. Protist., 87:97. Lemmermann, E. (1914) Pantostomatinae. Slisswasserflora Deutsch-

Desowitz, R.
gallinae.

lands. Pt. 1. McKay, F. and Morehouse, N. F.: (1948) Studies on experimental blackhead infection in turkeys. J. Parasit., 34:137. Niimi, D.: (1937) Studies on blackhead. II. J. Japan. Soc. Vet. Sc,

16:183.

Pascher, A. (1925) Neue oder wenig bekannte Protisten. XV. Arch.

:

Protist., 50:486.

(1895) An infectious disease among turkeys caused by protozoa. Bull. Bur. Animal Ind., U. S. Dep. Agr., no. 8. (1910) Amoeba meleagridis. Science, 32:509. (1915) Further investigations into the etiology of the protozoan disease of turkeys known as blackheads, etc. J. Med. Res., 33:243. Tyzzer, E. E.: (1919) Developmental phases of the protozoan of "blackhead" in turkeys. Ibid., 40:1. (1920) The flagellate character and reclassification of the parasite producing "blackhead" in turkey, etc. J. Parasit., 6:

Smith, T.

124.

(1934) Studies on histomoniasis, etc. Proc. Am. Acad. Arts Sc, 69:189. and Fabyan, M.: (1920) Further studies on "blackhead" in turkeys, etc. J. Infect. Dis., 27:207. (1922) A further inquiry into the source of the virus in blackhead of turkeys, etc. J. Exper. Med., 35:791. Wenrich, D. H.: (1943) Observations on the morphology of Histomonas from pheasants and chickens. J. Morphol., 72:279.

Chapter

14

Order 2 Protomonadina Blochmann

and are composed whose affinities to one another are very incompletely known. The body is in many cases plastic, having no definite pellicle, and in some forms amoeboid. The method of nutrition is holozoic, or saprozoic (parasitic). Reproduction is, as a rule, by longitudinal fission, although budding or multiple fission has also been known to occur, while sexual reproduction, though reported in some forms, has not been
flagella

possess one or two THEa protomonads heterogeneous Protozoa, mostly

of
lot of

parasitic,

confirmed.

With 1 flagellum With collar

Collar enclosed in jelly Collar not enclosed in jelly

Family

Phalansteriidae

Without lorica With lorica Without collar

Free-living
Parasitic

Family 2 Codosigidae Family 3 Bicosoecidae (p. 341) Family 4 Oikomonadidae Family 5 Trypanosomatidae Family 6 Cryptobiidae Family 7 Amphimonadidae
(p. (p.

343) 344) 357) 358) 360) 362)

With 2 flagella With undulating membrane Without undulating membrane

Flagella equally long

(p.

(p.

Flagella unequally long

No

trailing flagellum

One

flagellum trailing

Family 8 Monadidae Family 9 Bodonidae

Phalansteriidae Kent
;

(p. (p.

Family

Genus Phalansterium Cienkowski. Small, ovoid one flagellum and a small collar; numerous individuals are embedded in gelatinous
substance, with protruding flagella; fresh water.

P. digitatum Stein (Fig. 138,

dendritic; fresh water

a). Cells

about

17ju

long; oval; colony

among

vegetation.

Family 2 Codosigidae Kent

Small flagellates; delicate collar surrounds flagellum; ordinarily sedentary forms; if temporarily free, organisms swim with flagellum directed backward; holozoic on bacteria or saprozoic; often colonial;
free-living in fresh water.

Feeding process (Lapage, 1925).

Stein; Astrosiga Kent). In;

Genus Codosiga Kent (Codonocladium

dividuals clustered at end of a simple or branching stalk fresh water.

339

340

PROTOZOOLOGY
About
11/x

C. utriculus Stokes (Fig. 138, b).

long; attached to fresh-

water plants.
C. disjuncta (Fromentel) (Fig. 138,
c).

In stellate clusters;

cells

about

15ju

long; fresh water.

a, Phalansterium digitatum, X540 (Stein); b, Codosiga X1340 (Stokes); c, C. disjuncta, X400 (Kent); d, Monosiga ovata, X800 (Kent); e, M. robusta, X770 (Stokes); f. Desmarella moniliformis, X800 (Kent); g, Protospongia haeckeli, X400 (Lemmermann) h, an individual of Sphaeroeca volvox, X890 (Lemmermann); i, Diplosiga francei, X400 (Lemmermann); j, D. socialis, X670 (France^.

Fig.

138.

utriculus,

Genus Monosiga Kent.

ally

Solitary; with or without stalk; occasionwith short pseudo podia; attached to freshwater plants. Several

species.

M. M.

ovata

K.

(Fig. 138, d). 5-15/x long;

e).

with a short stalk.

13m long; stalk very long. Genus Desmarella Kent. Cells united laterally to one another;
robusta Stokes (Fig. 138,

fresh water.

D. moniliformis K. (Fig. 138,/). Cells about 6ju long; cluster composed of 2-12 individuals; standing fresh water. D. irregularis Stokes. Cluster of individuals irregularly branching, composed of more than 50 cells; cells 7-1 1m long; pond water.

PROTOMONADINA
Genus Proterospongia Kent.
P. haeckeli K. (Fig. 138,
g).

341

Stalkless individuals

embedded irreg-

ularly in a jelly mass, collars protruding; fresh water.

Body

oval; 8m long; flagellum 24-32ju

similar to

long; 6-60 cells in a colony.

Genus Sphaeroeca Lauterborn. Somewhat

spheroidal; fresh water.
S. volvox L. (Fig.

the last

genus; but individuals with stalks and radiating; gelatinous mass

138, h)

Cells ovoid, 8-12ju long; stalk about

twice as long; flagellum long; contractile vacuole posterior; colony

82-200>

in diameter; fresh water.

collars;

Genus Diplosiga Frenzel {Codonosigopsis Senn). With 2

fresh water.

without lorica; a contractile vacuole; solitary or clustered (up to 4);

D. francei D.

Lemmermann

(Fig. 138, i).

With a short
15/x

pedicel; 12ju

long; flagellum as long as body.

socialis F. (Fig. 138, j).

Body about

long; usually 4 clus-

tered at one end of stalk (15ju long).

Family 3 Bicosoecidae Poche

Small monomastigote; with lorica; solitary or colonial; collar may be rudimentary; holozoic; fresh water. Taxonomy and morphology
(Grasse and Deflandre, 1952). Genus Bicosoeca James-Clark. With vase-like lorica; body small,

ovoid with rudimentary collar, a flagellum extending through it; protoplasmic body anchored to base by a contractile filament (flagellum?); a nucleus and a contractile vacuole; attached or free-

swimming.
B. socialis Lauterborn (Fig. 139,
12^;
a).

Lorica cylindrical,

23/x

by

body about 10>

long; often in groups; free-swimming in fresh

water.

B. kepneri Reynolds. Body pyriform: 10m by 6m; lorica about 1.5 times the body length; flagellum about 30m long (Reynolds, 1927). Genus Salpingoeca James-Clark. With a vase-like chitinous lorica to which stalked or stalkless organism is attached; fresh or salt
water.

Numerous

species (Pascher, 1925, 1929).

Morphology (Hofe-

neder, 1925).
S. fusiformis Kent (Fig. 139, 6). Lorica short vase-like, about 1516m long; body filling lorica; flagellum as long as body; fresh water. Genus Diplosigopsis France. Similar to Diplosiga but with
lorica; solitary; fresh

water on algae.
(Fig.

D.

affinis

Lemmermann

139,

c).

form, about 15^ long;

body not

filling lorica; fresh

Chitinous lorica, spindlewater.

342

PROTOZOOLOGY
lorica;

Genus Histiona Voigt. With

filament; anterior end with lips

but body without attaching

water.

and

sail-like projection; fresh

Morphology (Pascher,

1943).

H. zachariasi V. (Fig. 139, d). Lorica cup-like; without stalk; about 13/a long; oval body 13/x long; flagellum long; standing fresh
water.

Genus Poteriodendron

Stein. Similar to Bicosoeca;

but colonial;

fusiformis,

a, Bicosoeca socialis, X560 (Lauterborn); b, Salpingoeca X400 (Lemmermann); c, Diplosigopsis affinis, X590 (France^; d, Histiona zachariasi, X440 (Lemmermann); e, Poteriodendron petiolatunij X440 (Stein); f, Codonoeca inclinata, X540 (Kent); g, Lagenoeca ovata, X400 (Lemmermann).

Fig.

139.

lorica vase-shaped:

with a prolonged stalk; fresh water. Flagellar

Lorica 17-50^ high; body 21-35/t

movement

(Geitler, 1942).
(S.) (Fig. 139, e).

P. petiolatum

long; flagellum twice as long as body; contractile vacuole terminal;

standing fresh water.

Genus Codonoeca James-Clark. With a stalked

C. inclinata

lorica; a single

flagellum; 1-2 contractile vacuoles; fresh or salt water.

Kent

(Fig.

139, /). Lorica oval; aperture truncate;

about 23m long; stalk twice as long; body oval, about 17m long; flagellum 1.5 times as long as body; contractile vacuole posterior;
standing fresh water.
lorica;

Genus Lagenoeca Kent. Resembles somewhat Salpingoeca; with but without any pedicel between body and lorica; solitary;
L. ovata

free-swimming; fresh water.

Lemmermann

(Fig. 139, g). Lorica oval, 15/x long;

body

loosely filling lorica; flagellum 1.5 times

body

length; fresh water.

Genus Stelexomonas Lackey.

single collar longer

than body;

PROTOMONADINA

343

vesicular nucleus median; a contractile vacuole terminal; individuals

are enclosed in arboroid, dichotomously branching tubes; fresh

water.
S. dichotoma L. (Fig. 140, a). Body ovoid, 10m by 8m; flagellum up to 25/x long; collar 12m long; the dichotomous tube infolded and wrinkled where branched; organisms are not attached to the tube

(Lackey, 1942).

a, Stelexomonas dichotoma, X1000 (Lackey); b, Oikomonas X1330 (Lemmermann) c, Thylacomonas compressa, X640 (Lemmermann); d, Ancyromonas contorta, X2000 (Lemmermann); e, Platytheca microspora, X650 (Stein): f, Aulomonas purdyi, X1000 (Lackey); g, Caviomonas mobilis, X2400 (Nie).

Fig. 140.

termo,

Family 4 Oikomonadidae Hartog

Genus Oikomonas Kent. A rounded monomastigote; uninucleate; encystment common; stagnant water, soil and exposed faecal matter. Several workers note the affinity of the members of this genus
with Chrysomonadina, on the basis of general structure, cyst, etc., though lacking chromatophores. Owen (1949) points out the flagel-

lum

of

Oikomonas

is

a simple one, typical of Chrysomonadina.

0. termo (Ehrenberg) (Fig. 140, b). Spherical or oval; anterior end

lip-like;

flagellum about twice

5-20m

in diameter;

body length; a contractile vacuole; stagnant water. Bacteria-free culture (Hardin,

Pellicle distinct;

1942); bacterial food (Hardin, 1944, 1944a).

Genus Thylacomonas Schewiakoff.

cytostome

344

PROTOZOOLOGY
by
18/x;

anterior; one flagellum; contractile vacuole anterior; rare.

T. compressa S. (Fig. 140, c). 22/u

flagellum

body length;

fresh water.

Genus Ancyromonas Kent. Ovate

vibratile

to triangular;

free-swimming or
its distal

adherent; flagellum trailing, adhesive or anchorate at

end,

throughout remainder of
d).

its

length; nucleus central; a

contractile vacuole; fresh or salt water.

A. contorta (Klebs) (Fig. 140,

Triangular, flattened; posterior

end pointed;

6-7/z

by

5-6/n; flagellum short;

a contractile vacuole;

standing fresh water.

Genus Platytheca
small aperture;
1

Stein.

With a

flattened pyriform lorica, with a

or more contractile vacuoles; fresh water.

S.

P. microspora

(Fig.

140, e). Lorica yellowish

brown, with a
roots of

small aperture; 12-18/x long; flagellum short;

among

Lemna.
but

Genus Aulomonas Lackey.

not attached
to,

Solitary

and

colorless; enclosed in,

a thin hyaline cylindrical tube, which expands like a

funnel at one end and broken at the other end; fresh water.

A. purdyi L. (Fig. 140,/). Ovoid, 6-8ju by 4-5/x; flagellum 10-16m

long; nucleus median; one contractile vacuole at each end of the

body (Lackey, 1942). Genus Caviomonas Nie. Elongate pyriform; a

single flagellum

from the rounded anterior end where a vesicular nucleus is located; a band-like "peristyle" runs along the body; without cytostome;
parasitic.

One

species (Nie, 1949).

C. mobilis
3ju; in

(Fig. 140, g). Body 2.2-6.6/x by 2-3m; average 4/x by addition to the peristyle, a short, fine spinous strand occurs;

N.

in the caecal contents of guinea-pig, Cavia porcella.

Family 5 Trypanosomatidae Doflein

Body
arises

characteristically leaf-like,

extent; a single nucleus

(Figs.
9;

though changeable to a certain and a blepharoplast from which a flagellum

141);

basal portion of the flagellum forms the

outer margin of undulating

of body; exclusively parasitic; a

membrane which extends along one side number of important parasitic

Protozoa which are responsible for serious diseases of man and domestic animals in various parts of the world are included in it.

Morphology and taxonomy (Grass6, 1952). Genus Trypanosoma Gruby. Parasitic in the circulatory system of vertebrates; highly flattened, pointed at flagellate end, and bluntly rounded, or pointed, at other; polymorphism due to differences in
development common; nucleus central; near aflagellate end, there is a blepharoplast from which the flagellum arises and runs toward

PROTOMONADINA
opposite end,

345

marking the outer boundary of the undulating most cases fiagellum extends freely beyond body; many with myonemes; multiplication by binary or multiple fission. The organism is carried from host to host by blood-sucking invertebrates and undergoes a series of changes in the digestive system of the latter (Fig. 142). A number of forms are pathogenic to their hosts and the diseased condition is termed trypanosomiasis in general.

membrane;

in

In vertebrate host

346

PROTOZOOLOGY

numbers and these migrate back gradutowards proventriculus in which they become predominant forms. They further migrate to the salivary glands and attach themslender forms appear in great
ally

lus fasciatus

life-cycle of Trypanosoma lewisi in the flea, Ceratophyl(Minchin and Thomson, modified), a, trypanosome from rat's blood; b, individual after being in flea's stomach for a few hours; o-l, stages in intracellular schizogony in stomach epithelium; m-r, two ways in which rectal phase may arise from stomach forms in rectum; s, rectal phase, showing various types; t, secondary infection of pylorus of hind-gut, showing forms similar to those of rectum.

Fig. 142.

The

PROTOMONADINA
selves to the duct-wall in crithidia form.

347

Here the development conand the flagellates finally transform themselves into small trypanosomes which are now infective. These metacyclic trypanosomes pass down through the ducts and hypopharynx. When the fly bites a person, the trypanosomes enter the victim. In addition
tinues for 2-5 days
to this so-called cyclic transmission, mechanical transmission

may

take place.

Trypanosoma gambiense

is

Gambian or Central African

sleeping sickness.

a pathogenic protozoan which causes The disease occurs in,

Fig. 143. a-d, Trypanosoma gambiense; e-h, T. rhodesiense, in stained blood smears of experimental rats, X2300. An erythrocyte of rat is shown for comparison, a, b, typical forms; c, d, division stages; e, f, typical forms; g, h, post-nuclear forms.

and confined to, central Africa within a zone on both sides of the equator where the vectors, Glossina palpalis and G. tachinoides (on the west coastal region) live. Many wild animals have been found naturally infected by the organisms and are considered to be reservoir hosts.
of the

Among

the domestic animals, the pigs appear to be one

most

significant, as

they themselves are said not to suffer from

infection.

The

chief lesions of infection are in the lymphatic glands

all cases,

the central nervous system. In

there

is

and in an extensive small-

348
cell infiltration of

PROTOZOOLOGY
the perivascular lymphatic tissue throughout the

central nervous system.

T. rhodesiense Stephens

and Fantham

(Fig. 143, e-h).

Morphologi-

cally similar to T. gambiense, but

when inoculated

into rats, the posi-

tion of the nucleus shifts in certain proportion (usually less than

of individuals
plast,

5%)

toward the posterior end, near or behind the blepharo-

together with the shortening of body.

Some

consider this
of T. brucei.

trypanosome as a virulent race of T. gambiense or one transmitted

by a different vector, others consider it a human strain The disease caused by this trypanosome appears
virulent

to be more and runs a course of only a few months. It is known as Rhodesian or East African sleeping sickness. The organism is confined to south-eastern coastal areas of Africa and transmitted by

Glossina morsitans.
T. cruzi

Chagas (Schizotrypanum

cruzi

C).

(Fig. 144).

small

Fig. 144.

Trypanosoma

cruzi in experimental rtas. a-c, flagellate forms

in blood; d, e, cytozoic forms, all

X2300;

f,

a portion of infected cardiac

muscle, X900.

curved (C or U) form about 20m long; nucleus central; blepharoplast conspicuously large, located close to sharply pointed non-flagellate end; multiplication takes place in the cells of nearly every organ of the host body; upon entering a host cell, the trypanosome loses its flagellum and undulating membrane, and assumes a leishmania form which measures 2 to by. in diameter; this form undergoes repeated binary fission, and a large number of daughter individuals are produced; they develop sooner or later into trypanosomes which, through rupture of host cells, become liberated into blood stream.
Life cycle (Elkeles, 1951).

This trypanosome is the causative organism of Chagas' disease or South American trypanosomiasis which is mainly a children's disease, and is widely distributed in South and Central America and as

PROTOMONADINA
far north as

349

North America. In the infected person, the show minute cyst-like bodies. The transmission of the organism is carried on apparently by numerous species of reduviid bugs, bed bugs and certain ticks, though the first named bugs belonging to genus Triatoma (cone-nosed or
Mexico
in

heart and skeletal muscles

kissing bugs) especially T. megista (Panslrongylus megistus), are the

chief vectors.

When

P. megistus

(nymph

or adult) ingests the in-

fected blood, the organisms undergo division in the

intestine,

stomach and

and become transformed into

crithidia

forms which con-

tinue to multiply. In eight to 10 days the metacyclic or infective trypanosomes make their appearance in the rectal region and pass out in the faeces of the bug at the time of feeding on host. The parasites gain entrance to the circulatory system when the victim scratches the bite-site or through the mucous membrane of the eye (Brumpt, 1912; Denecke and von Haller, 1939; Weinstein and Pratt,
1948).

wood

Cats, dogs, opossums, monkeys, armadillos, bats, foxes, squirrels, rats, etc., have been found to be naturally infected by T. cruzi,

hosts. Vectors are also numerous. have been reported from the United States, but Wood (1934) found a San Diego wood rat (Neotoma fuscipes macrotis) in the vicinity of San Diego, California, infected by Trypanosoma cruzi and Packchanian (1942) observed in Texas, 1 nine-banded armadillo (Dasypis novemcinctus) 8 opossums (Didelphys virginiana), 2 house mice (Mus musculus), and 32 wood rats {Neotoma micropus micropus), naturally infected by Trypanosoma cruzi. It has now become known through the studies of Kofoid, Wood, and others that Triatoma protracta (California, New Mex-

and are considered as reservoir

No

cases of Chagas' disease

ico),

T. rubida (Arizona, Texas), T. gerstaeckeri (Texas), T. heide-

manni (Texas), T. longipes (Arizona), etc., are naturally infected by T. cruzi. Wood and Wood (1941) consider it probable that

human

may exist in southwestern United from a naturally infected Triatoma heidemanni were shown by Packchanian (1943) to give rise to a typical Chagas' disease in a volunteer. Reduviid bugs (Usinger, 1944) Chagas' disease in the United States (Packchanian, 1950) in
cases of Chagas' disease
States. In fact, the organisms
;

central Brazil (Dias, 1949).

T.brucei Plimmer and

Bradford (Fig. 145,

all

a).

Polymorphic;

15-30ju long (average 20/x); transmitted

flies,

by various

species of tsetse

Glossina; the most virulent of

trypanosomes; the cause of

the fatal disease

camels, cattle,

"nagana" among mules, donkeys, horses, swine, dogs, etc., which terminates in the death of

known

as

350

PROTOZOOLOGY

the host animal in from two weeks to a few months; wild animals are equally susceptible; the disease occurs, of course, only in the
region in Africa where the tsetse
T. theileri
flies live.

Laveran

(Fig. 145, b).

Large trypanosome which oc-

curs in blood of cattle; sharply pointed at both ends; 60-7 0/t long;

myonemes
1918). T.

are well developed. Cytology

(Hartmann and

Noller,

americanum Crawley. In American

cattle; 17-25/u or longer;

only crithidia forms develop in culture. Crawley (1909, 1912) found it in 74 per cent and Glaser (1922a) in 25 per cent of cattle they

examined. The latter worker considered that this organism was an intermediate form between Trypanosoma and Crithidia.

d,

Fig. 145. a, Trypanosoma brucei; b. T. theileri; c, T. melophagium T. evansi; e, T. equinum; f, T. equiperdum; g, T. lewisi; all X1330 (several authors).

T. melophagium (Flu) (Fig. 145, c). A trypanosome of the sheep; 50-60m long with attenuated ends; transmitted by Melophagus
ovinus.

T. evansi (Steel) (Fig. 145, d). In horses, mules, donkeys, cattle, dogs, camels, elephants, etc.; infection in horses seems to be usually fatal and known as "surra"; about 25/x long; monomorphic; trans-

mitted by tabanid
1928).

flies;

widely distributed. Transmission (Nieschulz,

e).

T. equinum Vages (Fig. 145,

In horses in South America, caus-

known as "mal de Caderas"; other domestic animals do not suffer as much as do horses; 20-25/* long; without
ing an acute disease

blepharoplast.

PROTOMONADINA
T. equiperdum Doflein (Fig.

351

145, /). In horses and donkeys; causes "dourine," a chronic disease; widely distributed; 25-30> long; no intermediate host; transmission takes place directly from host to host during sexual act. Nuclear division (Roskin and Schisch.,

1928).

hippicum Darling. In horses and mules in Panama; the cause "murrina" or "derrengadera"; 16-18/x long; posterior end obtuse; mechanically transmitted by flies; experimentally various domestic and wild animals are susceptible, but calf is refractory (Darling, 1910, 1911). Serological tests (Taliaferro and Taliaferro, 1934). T. lewisi (Kent) (Figs. 142; 145, g). In the blood of rats; widely distributed; about 30m long; body slender with a long flagellum; transmitted by the flea Ceratophyllus fasciatus, in which the organism undergoes multiplication and form change (Fig. 142); when a rat swallows freshly voided faecal matter of infected fleas containing the metacyclic organisms, it becomes infected. Many laboratory animals are refractory to this trypanosome, but guinea pigs are susceptible (Laveran and Mesnil, 1901: Coventry, 1929). Variation and inheritance of size (Taliaferro, 1921, 1921a, 1923); reproductionT.
of

inhibiting reaction product (Taliaferro, 1924, 1932)

nuclear division

(Wolcott, 1952).
T. neotomae

Wood

(?

T. triatomae Kofoid

and McCulloch). In
f.

wood

rats,

Neotoma fuscipes annectens and N.

macrotis; resembles

29m long; blepharoplast large, rod-form; free flagellum relatively short; the development in the vector flea Orchopeas
T. lewisi; about

W. wickhami,
Wood,

similar to that of T. lewisi; experimentally

Norway
D.

rats are refractory (and

wood

rats are refractory to T. lewisi (Fae

morphology of trypanosomes which occur in California rodents and shrews (Davis, 1952). T. duttoni Thiroux. In the mouse; similar to T. lewisi, but rats are said not to be susceptible, hence considered as a distinct species; transmission by fleas. Antibodies (Taliaferro, 1938). T. peromysci Watson. Similar to T. lewisi; in Canadian deer mice, Peromyscus maniculatus and others. T. nabiasi Railliet. Similar to T. lewisi; in rabbits, Lepus domesticus and L. cuniculus. T. paddae Laveran and Mesnil. In Java sparrow, Munia oryzi1936)); comparative
vora.

T. noctuae (Schaudinn). In the

owl Athene noctua.

(Novy and MacNeal, 1905; Laveran and Mesnil, 1912; Wenyon, 1926). Crocodiles, snakes and turtles are also hosts for trypanosomes (Roudabush and Coatney,
species occur in birds

Numerous other

352
1937). Transmission
T. rotatorium

PROTOZOOLOGY

is by blood-sucking arthropods or leeches. (Mayer) (Fig. 146, a). In tadpoles and adults of various species of frog; between a slender form with a long projecting flagellum measuring about 35/x long and a very broad one without free portion of flagellum, various intermediate forms are to be noted in a single host; blood vessels of internal organs, such as kidneys, contain more individuals than the peripheral vessels; nucleus central, hard to stain; blepharoplast small; undulating membrane

Fig. 146. a, Trypanosoma rotatorium X750 (Kudo); b, T. inopinatum, X1180 (Kudo); c, T. diemyctyli, XSOO (Hegner); d, T. giganteum, X500 (Neumann); e, T. granulosum, XlOOO (Minchin); f, T. remaki, X1650 (Kudo); g, T. percae, XlOOO (Minchin); h, T. danilewskyi, XlOOO (Laveran and Mesnil); i, T. rajae, X1600 (Kudo).

highly developed;

myonemes prominent;

multiplication

by

longi-

tudinal fission; the leech, Placobdella marginata, has been found to

be the transmitter in some localities T. inopinatum Sergent and Sergent (Fig. 146, b). In blood of various frogs; slender; 12-20/x long; larger forms 30-35/z long; blepharoplast comparatively large; transmitted by leeches. Numerous species of Trypanosoma have been reported from the
frog,

but

specific identification is difficult; it is better

and

safer

to hold that they belong to

one of the 2 species mentioned above until their development and transmission become known. T. diemyctyli Tobey (Fig. 146, c). In blood of the newt, Triturus viridescens ; a comparatively large form; slender; about 50ju by 2-5ju; flagellum 20-25/n long; with well developed undulating membrane.

PROTOMONADINA
Both
fresh

353

and salt water fish are hosts to different species of trypanosomes; what effect these parasites exercise upon the host fish is not understood; as a rule, only a few individuals are observed in the peripheral blood of the host. Transmission (Robertson,
1911); species (Laveran
1951).
T.

and Mesnil, 1912; Wenyon, 1926; Laird,

(Fig. 146, e). In the eel, Anguilla

vulgaris;

granulosumL&ver&n and Mesnil 70-80> long.

T. giganteum

Neumann

(Fig. 146, d).

In Raja oxyrhynchus; 125-

130^ long. T. remaki Laveran and Mesnil (Fig. 146, /). In Esox lucius, E. reticulatus and probably other species; 24-33/x long. (Kudo, 1921).
(Fig. 146, g). In Perca fluviatilis; 45-50> long. Laveran and Mesnil (Fig. 146, h). In carp and goldfish; widely distributed; 40> long. T. rajae Laveran and Mesnil (Fig. 146, i). In various species of Raja; 30-35/x long (Kudo, 1923). Genus Crithidia Leger. Parasitic in arthropods and other invertebrates; blepharoplast located between central nucleus and flagellumbearing end (Fig. 141); undulating membrane not so well developed as in Trypanosoma; it may lose the flagellum and form a leptomonas or rounded leishmania stage which leaves host intestine with faecal matter and becomes the source of infection in other host animals. C. euryophthalmi McCulloch (Fig. 147, a-c). In gut of Eury-

T. percae

Brumpt

T. danilewskyi

ophthalmus convivus; California coast. C. gerridis Patton (Fig. 147, d). In intestine of water bugs, Gerris

and Microvelia; 22-45^

migis. C.

long.

Becker (1923) saw

147,
in
e, /).

this in Gerris re-

hyalommae O'Farrell
is

(Fig.

cattle tick,
its

Hyalomma aegyptium
in the

Egypt; the

In body cavity of the flagellate through

invasion of ova
it is still

said to be capable of infecting the offspring

in invertebrates;

while

body of the parent tick. Genus Leptomonas Kent. Exclusively parasitic

;

blepharoplast very close to flagellate end without undulating brane (Fig. 141); non-flagellate phase resembles Leishmania.
L. ctenocephali
flea,

mem-

Fantham

(Fig. 147,

g,

h).

In hindgut of the dog

Ctenocephalus canis; widely distributed. Morphology (Yama-

saki, 1924).

Genus Phytomonas Donovan. Morphologically similar to Leptomonas (Fig. 141); in the latex of plants belonging to the families Euphorbiaceae, Asclepiadaceae, Apocynaceae, Sapotaceae and Utricaceae; transmitted by hemipterous insects; often found in

354

PROTOZOOLOGY

enormous numbers in localized areas in host plant; infection spreads from part to part; infected latex is a clear fluid, owing to the absence of starch grains and other particles, and this results in degeneration
of the infected part of the plant. Several species.

P. davidi (Lafront). 15-20> by about 1.5/z; posterior portion of body often twisted two or three times; multiplication by longitudinal fission; widely distributed; in various species of Euphorbia.

P. elmassiani (Migone) (Fig. 147,

i,

j).

In various species of milk

Fig. 147. a-c, Crithidia euryophthalmi

(a, b,

in mid-gut;
e,

c,
f,

in rectum),

C. hyalomLeptomonas ctenocephali, XlOOO (Wenyon); i, j, Phytomonas elmassiani (i, in milkweed, Asclepias sp. j, in gut of a suspected transmitter, Oncopeltus fasciatus), X1500 (Holmes); k, Herpetomonas muscarum, X1070 (Becker); 1-n, H. drosophilae, XlOOO (Chatton and Leger). C. gerridis,
g, h,
;

X880 (McCulloch); d, mae, X1000 (O'Farrell);

X1070 (Becker);

weeds; 9-20/x long; suspected transmitter, (Holmes, 1924); in South and North America.

Oncopeltus fasciatus

genus (Fig. 141); exTrypanosoma-, Crithidia-, Leptomonas-, and Leishmania-forms occur during development. Several
Ill-defined

Genus Herpetomonas Kent.

clusively invertebrate parasites;

species. Species in insects

(Drbohlav, 1925).
(Fig. 147, k).

H. muscarum (Leidy) (H. muscae-domeslicae Burnett)

In the digestive tube of
flies

belonging to the genera: Musca, Cal-

liphora, Cochliomyia, Sarcophaga, Lucilia,

by

2-3/x. Effect

Phormia, etc.; up to 30ju on experimental animals (Glaser, 1922) comparative

;

study (Becker, 1923a). H. drosophilae (Chatton and Alilaire) (Fig. 147, l-n). In intestine of Drosophila confusa; large leptomonad forms 21-25/u long, flagellum body-length; forms attached to rectum 4-5m long.

PROTOMONADINA

355

Genus Leishmania Ross. In man or dog, the organism is an ovoid body with a nucleus and a blepharoplast; 2-5;u in diameter; with vacuoles and sometimes a rhizoplast near the blepharoplast; intracellular parasite in the cells of reticuloendothelial

system; multi-

plication

by binary

fission.

In the intestine of blood-sucking insects

leptomonad which multiplies by longitudinal fission. Nuclear division (Roskin and Romanowa, 1928). There are known at present three "species" of Leishmania which are morphologically alike. They do not show any distinct differential characteristics either by animal inoculation experiments or by culor in blood-agar cultures, the organism develops into
(Fig. 148, d-j)

form

ture

method

or agglutination test.

Species of Phlebotomus (sand-flies) have long been suspected as

vectors of Leishmania.
patient,

When

a Phlebotomus feeds on kala-azar

the leishmania bodies become flagellated and undergo

multiplication so that
are large
flagellates

numbers

by the third day after the feeding, there Leptomonas flagellates in the mid-gut. These migrate forward to the pharynx and mouth cavity on the
of

is fed a second be found in the proboscis. But the great majority of the attempts to infect animals and man by the bite of infected Phlebotomus have failed, although in a number of cases small numbers of positive infection have been reported. Adler and Ber (1941) have finally succeeded in producing cutaneous leishmaniasis in 5 out of 9 human volunteers on the site of bites by laboratory-bred P. papatasii which were fed on the flagellates of Leishmania tropica suspended in 3 parts 2.7% saline and 1 part defib rinated blood and kept at a temperature of 30C. Swaminath, Shortt and Anderson (1942) also succeeded in producing kala-azar infections in 3 out of 5 volunteers through the bites of infected P.

4th or 5th day.

On

the 7th to 9th days (after the fly

time), the organisms

may

L. donovani (Laveran

and Mesnil)

(L. infantum, Nicolle) (Fig. 148).

As seen
(1-3/x)

in stained spleen

or ovoid (24/x

puncture smears, the organism is rounded by 1.5-2.5/z); cytoplasm homogeneous, but

nucleus comparatively large, often
in a host cell varies

often with minute vacuoles;

spread out and of varied shapes; blepharoplast stains more deeply

and small; number of parasites

over 100.

from a few to

This is the cause of kala-azar or visceral leishmaniasis which is widely distributed in Europe (Portugal, Spain, Italy, Malta, Greece,

and southern Russia),

in Africa

Abyssinia, Sudan, northern

Kenya and

(Morocco, Algeria, Tunisia, Libya, Nigeria), in Asia (India,

356

PROTOZOOLOGY

China, Turkestan, etc.), and in South America. The parasite is most abundantly found in the macrophages, mononuclear leucocytes, and polymorphonuclears of the reticulo-endothelial system of various organs such as spleen, liver, bone marrow, intestinal mucosa, lymphatic glands, etc. The most characteristic histological change appears to be an increase in number of large macrophages and mononuclears. The spleen and liver become enlarged due in part to increased fibrous tissue and macrophages.

Fig. 148. Leishmania donovani, X1535. a, an infected polymorphonuclear leucocyte; b, organisms scattered in the blood plasm; c, an infected monocyte; d-f, flagellate forms which develop in blood-agar cultures.

media (p. 886). becomes larger and elongate until it measures 14-20/z by 2/i. A flagellum as long as the body develops from the blepharoplast and it thus assumes leptomonad form (Fig. 148, /) which repeats longitudinal division. Dogs are naturally infected with L. donovani and may be looked upon as a reservoir host. Vectors are Phlebotomus argentipes and other species of Phlebotomus. L. tropica (Wright). This is the causative organism of the Oriental sore or cutaneous leishmaniasis. It has been reported from Africa (mainly regions bordering the Mediterranean Sea), Europe (Spain Italy, France, and Greece), Asia (Syria, Palestine, Armenia, Southern Russia, Iraq, Iran, Arabia, Turkestan, India, Indo-China, and China), and Australia (northern Queensland). The organisms are present in the endothelial cells in and around the cutaneous lesions, located on hands, feet, legs, face, etc. L. tropica is morphologically indistinguishable from L. donovani, but some believe that it shows a wider range of form and size than the latter. In addition to rounded or ovoid forms, elongate forms are
is

The organism

easily cultivated in blood-agar

After two days,

it

PROTOMONADINA
the scrapings of lesions.
tasii (p. 355),

357

often found, and even leptomonad forms have been reported from

The

insect vectors are Phlebotomus papa-

P. scrgenti and others. Direct transmission through

wounds

in the skin also takes place.

it

The

lesion appears first as a

small papula on skin;

increases in size

Microscopically an infiltration of
cytes and macrophages
is

and later becomes ulcerated. corium and its papillae by lympho-

noticed; in ulcerated lesions leishmania

bodies are found in the peripheral zone and below the floor of the
ulcers.

L. brasiliensis Vianna. This organism causes Espundia, Bubos, or American or naso-oral leishmaniasis, which appears to be confined to South and Central America. It has been reported from Brazil, Peru, Paraguay, Argentina, Uruguay, Bolivia, Venezuela, Ecuador, Colombia, Panama, Costa Rica, and Mexico.
Its

tropica,

morphological characteristics are identical with those of L. and a number of investigators combine the two species into

However, L. brasiliensis produces lesions in the mucous membrane of the nose and mouth. Vectors appear to be Phlebotomus intermedins, P. panamensis and other species of the genus. Direct
one.

transmission through

wounds

is

also possible. Fuller

and Geiman

(1942) find Citellus tridecemlineatus a suitable experimental animal.

Family 6 Cryptobiidae Poche

Biflagellate trypanosome-like pro to monads;
1

flagellum free, the

other marks outer margin of undulating membrane; blepharoplast

an elongated rod-like structure, often referred to as the parabasal body; all parasitic. Genus Cryptobia Leidy (Trypanoplasma Laveran and Mesnil). Parasitic in the reproductive organ of molluscs (Leidy, 1846) and
other invertebrates; also in the blood of fishes.
C. helicis L. (Fig. 149, a-c). In the reproductive organ of various

species of

pulmonate

snails:

Triodopsis albolabris,

T.

tridentata,

Anguispira alternata (Leidy, 1846), Helix aspersa, and Monadenia

fidelis (Kozloff,

1948); 16-26.5 M by 1.5-3.3/x.

Morphology and

cul-

ture (Schindera, 1922).

C. borreli (Laveran and Mesnil) (Fig. 149, d, e). In blood of various freshwater fishes such as Catostomus, Cyprinus, etc.; 20-25/x long

(Mavor, 1915).
C. cyprini (Plehn) (Fig. 149, /).
10-30/z long; rare.

In blood of carp and goldfish;

C. grobbeni (Keysselitz). In coelenteric cavity of Siphonophora;

about

65/x

by

4/x.

358

PROTOZOOLOGY
Family
7

Amphimonadidae Kent

or with a gelatinous envelope; 2 equally long anterior flagella; often colonial; 1-2 contractile vacuoles; free-swimming or

Body naked
;

attached mainly fresh water.

Genus Amphimonas Dujardin. Small oval or rounded amoeboid; flagella at anterior end; free-swimming or attached by an elongated
stalk-like posterior process; fresh or salt water.

helicis,

a neutral red stained and b, a fixed and stained Cryptobia (Kozloff); c, stained specimen of the same organism, X1690 (Belaf); d, a living and e, stained C. borreli, X1730 (Mavor); f, C. cyprini, X600 (Plehn).
Fig. 149.
a,

X2200

A. globosa Kent (Fig. 150,

a).

Spherical; about 13/x in diameter;

stalk long, delicate; fresh water.

Genus Spongomonas
pseudopodia

Stein. Individuals in granulated gelatinous

masses; 2 flagella; one contractile vacuole; colonial; with pointed

in motile stage; fresh water.

S. uvella S. (Fig. 150, 6). Oval; 8-12/x long; flagella 2-3 times as

long; colony about 50ju high; fresh water.

Genus Cladomonas Stein. Individuals are embedded in dichotomous dendritic gelatinous tubes which are united laterally; fresh
water.
C. fruticulosa S. (Fig. 150,
85ju high.
c).

Oval; about 8^ long; colony up to

Genus Rhipidodendron
;

Stein. Similar to Cladomonas,

but tubes

are fused lengthwise fresh water.

PROTOMONADINA

359

R. splendidum S. (Fig. 150, d, e). Oval; about 13m long; flagella about 2-3 times body length; fully grown colony 350/z high. Genus Spiromonas Perty. Elongate; without gelatinous covering;
spirally twisted; 2 flagella anterior; solitary; fresh water. S. augusta (Dujardin) (Fig. 150,/). Spindle-form;

about

10ju

long;

stagnant water.

globosa, X540 (Kent); b, Spongomonas uvella, Cladomonas fruticulosa, X440 (Stein); d, e, Rhipidodendron splendidum (d, a young colony, X440; e, a freeswimming individual, X770) (Stein); f, Spiromonas augusta, X1000 (Kent); g, Diplomita soci-

Fig. 150.

a,

Amphimonas
c,

X440

(Stein);

alis,

X1000 (Kent); h, Streptomonas Dinomonas vorax, X800 (Kent).

cordata,

X890 (Lemmermann)

i,

to

Genus Diplomita Kent. With transparent lorica; body attached bottom of lorica by a retractile filamentous process; a rudimen(?)
;

tary stigma

fresh water.
(Fig. 150, g).

D.

socialis

K.

body length;
about

lorica yellowish or pale

Oval flagellum about 2-3 times the brown; broadly spindle in form;
distinctly

15ju long; pond water. Genus Streptomonas Klebs. Free-swimming; naked;

keeled; fresh water.

S. cordata (Perty) (Fig. 150, h).

Heart-shaped;

15/u

by

13/*;

rota-

tion

movement,

360

PROTOZOOLOGY
plastic, free-swim-

Genus Dinomonas Kent. Ovate or pyriform,

ming; 2 fiagella, equal or sub-equal, inserted at anterior extremity, where large oral aperture, visible only at time of food ingestion, is also located, feeding on other flagellates; in infusions. D. vorax K. (Fig. 150, i). Ovoid, anterior end pointed; 15-16ju. long; fiagella longer than body; hay infusion and stagnant water.

Family 8 Monadidae Stein

Two

unequal

fiagella;

one primary and the other secondary; swimcontractile vacuoles; colony formation fre-

ming or attached; 1-2

quent; free-living.

often attached to foreign objects; small,

salt water.

Genus Monas Muller (Physomonas Kent). Active and plastic; up to 20m long; fresh and

Some authors hold

that this genus should be placed in

for

Chrysomonadina on the same ground mentioned

343). Flagellar

Oikomonas

(p.

movement (Krijgsman, 1925); cyst morphology and taxonomy (Reynolds, 1934).

(Scherffel, 1924);

M.

guttula

Ehrenberg

(Fig.

151, a). Spherical to ovoid;

14-16m

long; free-swimming or attached; longer flagellum about 1-2 times

body length; cysts 12m

in diameter;

stagnant water.

elongata (Stokes) (Fig. 151, b). Elongate; about 11m long; freeswimming or attached; anterior end obliquely truncate; fresh water.

M.

M. socialis (Kent) (Figs. 8, d; 151, c). Spherical; 5-10ju long; among decaying vegetation in fresh water. M. vestita (Stokes) (Fig. 151, d). Spherical; about 13.5m in diameter; stalk about 40m long; pond water. Reynolds (1934) made a
careful study of the organism.

Meyer. Body 8-10ju long by 5m; two unequal fiagella; as long as the body and the shorter one about onefourth; 20-50 individuals form a spheroid colony, resembling a detached colony of Anthophysis; polysaprobic.

M.

sociabilis

the longer one

is

Genus Stokesiella Lemmermann. Body attached by a fine cytoplasmic thread to a delicate and stalked vase-like lorica; 2 contractile

vacuoles; fresh water.

S. dissimilis (Stokes) (Fig. 151, e). Solitary; lorica S. leptostoma (S.) (Fig. 151, /). Lorica

about 28m long. about 17m long; often in

groups; on vegetation.

Genus Stylobryon Fromentel. Similar on algae in fresh water.

S. abbotti Stokes (Fig.

to Stokesiella;

but colonial

151, g). Lorica

campanulate; about 17m

fiagella

long;
short.

main

stalk about 100m high;

body oval or spheroidal;

PROTOMONADINA
Genus Dendromonas
Stein. Colonial; individuals

361

without

lorica,

located at end of branched stalks; fresh water

among
8/1

vegetation.

D. virgaria (Weisse) (Fig. 151,

high;

h).

About

long; colony 200/x

pond water.

X620 (Fisch); b, M. elongata, X670 X670 (Kent); d, M. vestita, X570 (Stokes); e, Stokesiella dissimilis, X500 (Stokes); f, S. leptostoma, X840 (Stokes); g, Stylobryon abbotti, X480 (Stokes); h, Dendromonas virgaria, a young Cephalothamnium cyclopum, X440 (Stein); colony of, X670 (Stein);
Fig.
151.
c,

a,

Monas

guttula,

(Stokes);

M.

socialis,

i,

j,

k,

Anthophysis vegetans
(Stein).

(j,

part of a colony,

X230;

k,

an individual,

X770)

Genus Cephalothamnium
fresh water. C. cyclopum S. (Fig. 151,

Stein. Colonial;

without
is

lorica,

but

in-

dividuals clustered at the end of a stalk which

colorless

and

rigid;

i).

Ovoid; 5-10/x long; attached to body

of Cyclops

and

also

among

plankton.

Genus Anthophysis Bory (Anthophysa). Colonial forms, somewhat similar to Cephalothamnium; stalks yellow or brownish and usually bent detached individuals amoeboid with pointed pseudo;

podia.

A. vegetans (Miiller) (Fig. 151,

j, k).

About 5-6m

long;

common

in

stagnant water and infusion.

362

PROTOZOOLOGY
Family 9 Bodonidae
Biitschli

With 2 flagella; one directed anteriorly and the other posteriorly and trailing; flagella originate in anterior end which is drawn out to a varying degree; one to several contractile vacuoles; asexual reproduction by binary fission; holozoic or saprozoic (parasitic). Morphology and taxonomy (Hollande, 1942, 1952). Genus Bodo Ehrenberg (Prowazekia Hartman and Chagas). Small, ovoid, but plastic; cytostome anterior; nucleus central or anterior; flagella connected with 2 blepharoplasts in some species; encystment common; in stagnant water and coprozoic. Numerous species. Cytology (Belaf, 1920; Hollande, 1936). B. caudatus (Dujardin) (Fig. 152, a, b). Highly flattened, usually tapering posteriorly; 11-22/x by 5-10>; anterior flagellum about body length, trailing flagellum longer; blepharoplast; cysts spherical;
stagnant water.
B. edax Klebs (Fig. 152, c). Pyriform with bluntly pointed ends; 11 15/x by 5-7m; stagnant water. Genus Pleuromonas Perty. Naked, somewhat amoeboid; usually

attached with trailing flagellum; active cytoplasmic movement;

fresh water.

P. jaculans P. (Fig. 152, d). Body 6-10> by about 5/z; flagellum 2-3 times body length; 4-8 young individuals are said to emerge from a spherical cyst; stagnant water. Genus Rhynchomonas Klebs (Cruzella Faria, da Cunha and Pinto). Similar to Bodo, but there is an anterior extension of body, in which one of the flagella is embedded, while the other flagellum trails; a single nucleus; minute forms; fresh or salt water; also some-

times coprozoic.
fresh water
e). Oval, flattened; 5 6/u by 2-3/x; and coprozoic. R. marina (F., C. and P.). In salt water. Genus Proteromonas Kunstler (ProwazekeUa Alexeieff). Elongated pyriform; 2 flagella from anterior end, one directed anteriorly and the other, posteriorly; nucleus anterior; encysted stage is remarkable in that it is capable of increasing in size to a marked de-

R. nasuta (Stokes) (Fig. 152,

gree; exclusively parasitic; in gut of various species of lizards. Species (Grasse, 1926, 1952).

P. lacertae (Grassi) (Fig. 152, /). Elongate, pyriform; 10-30> long, gut of lizards belonging to the genera Lacerta, Tarentola, etc. Genus Retortamonas Grassi {Embadomonas Mackinnon). Body
plastic, usually

pyriform or fusiform, drawn out posteriorly; a large

PROTOMONADINA

363

cytostome toward anterior end; nucleus anterior; 2 flagella; cysts pyriform or ovoid; parasitic in the intestines of various animals.

Taxonomy (Wenrich,

1932; Kirby

and Honigberg,

1950).
10/x)

R. gryllotalpae G. (Fig. 152, g). About 7-14;u (average in intestine of the mole cricket, Gryllotalpa gryllotalpa.

long;

Fig. 152. a, b, Bodo caudatus, X1500 (Sinton); c, B. edax, X1400 (Kiihn); d, Pleuromonas jaculans, X650 (Lemmermann); e, Rhinchomonas nasuta, X1800 (Parisi); f, Proteromonas lacertae, X2500 (Ktihn); g, Retortamonas gryllotalpae, X2000 (Wenrich); h, R. blattae, X2000 (Wenrich); i, R. intestinalis, X2000 (Wenrich); j, Phijllomitus undulans, X1000 (Stein); k, Colponema loxodes, X650 (Stein); 1, Cercomonas longicauda, X2000 (Wenyon); m, C. crassicauda, X2000 (Dobell).

R. blattae (Bishop) (Fig. 152, h).

About

6-9/x long; in colon of

cockroaches.
R. intestinalis (Wenyon and O'Connor) (Figs. 152, i; 153). Polymorphic, often pyriform or ovoid with drawn-out posterior end; 4-9ju

by 3-4ju; cytostome large, about 1/3 the body length

vesicular nucleus

364

PROTOZOOLOGY

with an endosome near anterior end; anterior flagellum as long as the body; posterior flagellum shorter, but thicker, in or near cytostome; cysts pyriform; 4.5-7/* long; a single nucleus and an oblong
area surrounded by
tine; trophozoites
fibril;

commensal

in the

lumen

of

human

intes-

and

also cysts occur in diarrhoeic faeces; of

com-

paratively rare occurrence. Varieties (Hogue, 1933, 1936).

R. caviae (Hegner and Schumaker, 1928). In the caecum of guineapigs; stained trophozoites

4-7 /* by 2.4-3.2/* (H. and

S.), 4.4-7.7/*

by

4-4.3/* (Nie, 1950); stained cysts 3.4-5.2/*

4.5-5.7/*

by

3.3-3.6/z (H.

and

S.),

by

3.4-3.7/* (Nie).

Fig.

153. Retortamonas intestinalis,

c,

O'Connor;
isms in

Dobell and O'Connor;

stained trophozoites;

e, e,

g,

X2300 (a, Kudo; f,

cyst in
life;

b,

d,

Wenyon and

life; c, d,

Jepps). a, b, organf, g, stained cysts.

Genus Phyllomitus Stein. Oval; highly plastic; cytostome large and conspicuous; 2 unequal flagella, each originates in a blepharoplast; fresh

water or coprozoic.

P. undulans S. (Fig. 152, j), Ovoid; 21-27/* long; trailing flagellum much longer than anterior one; stagnant water. Genus Colponema Stein. Body small; rigid; ventral furrow conspicuous, wide at anterior end; one flagellum arises from anterior end

and the other from middle of body; fresh water. C. loxodes S. (Fig. 152, k). 18-30/* by 14/* cytoplasm with
globules.

refractile

Genus Cercomonas Dujardin. Biflagellate, both flagella arising from anterior end of body; one directed anteriorly and the other runs backward over body surface, becoming a trailing flagellum; plastic; pyriform nucleus connected with the blepharoplast of flagella; spherical cysts uninucleate; fresh water or coprozoic.

PROTOMONADINA
C. longicauda D. (Fig. 152,
V).

365

drawn out;
fresh water

18-36/x

by

9-14ju; flagella as long as

Pyriform or ovoid; posterior end body; pseudo podia;

and coprozoic.

C. crassicauda D. (Fig. 152, m). 10-16ju

by

7-10/*; fresh

water and

coprozoic.

References

Adler, S. and Ber, M.: (1941) Transmission of Leishmtnia tropica by the bite of Phlebotomus papatasii. Indian J. Med. Research,
29:803.

Becker, E. R.

(1923) Observations on the morphology and life cycle of Crithidia gerridis, etc. J. Parasit., 9:141. (1923a) Observations on the morphology and life history of
:

Herpelomonas muscae-domesticae
flies.

in

North American muscoid

Protist.,

Ibid., 9:199.
:

Belar, K. (1920) Die Kernteilung von Prowazekia. Arch.

41:308.

Brumpt, E.: (1912) Penetration du Schizotrypanum cruzi a travers la muqueuse oculaire saine. Bull. Soc. Path. Exot., 5:723. Coventry, F. A. (1929) Experimental infections with Trypanosoma
:

lewisi in the guinea pigs.

Am.

J.

Crawley, H.:
Bull. Bur.

(1909) Studies on blood

Hyg., 9:247. and blood parasites. I III.

Animal Ind., U. S. Dep. Agr., no. 119. Trypanosoma americanum, a common blood parasite of American cattle. Ibid., no. 145. Darling, S. T. (1910) Equine trypanosomiasis in the canal zone.
(1912)
:

Bull. Soc. Path. Exot., 3:381. (1911) Murrina: etc. J. Infect. Dis., 8:467.

Davis, Betty
fornia

S.: (1952) Studies on the trypanosomes of some Calimammals. Univ. California Publ. Zool., 57:145. Denecke, K. and Haller, E. v.: (1939) Recherches experimentale

sur le

mode de

Trypanosoma
Dias, E.
:

transmission et le course de l'infection par cruzi chez les souris. Ann. Parasit., 17:313.

(1949) Consideracoes sobre a doenca de Chagas. Mem. Oswaldo Cruz, 47:679. Drbohlav, J.: (1925) Studies on the relation of insect flagellates to
Inst.

Leishmaniasis. I III.
Parasit., 37:379.

Am.

J.

Hyg., 5:580.
cycle of

Elkeles, G.: (1951) On the

life

Trypanosoma

cruzi.

J.

Fuller, H.

S. and Geiman, Q. M.: (1942) South American cutaneous leishmaniasis in experimental animals. J. Parasit., 28:429. Geitler, L.: (1942) Beobachtungen liber die Geisselbewegung der Bicoecacee Poteriodendron. Arch. Protist., 96:119. Glaser, R. W.: (1922) Hcrpetomonas muscae-domesticae, its behavior and effect in laboratory animals. J. Parasit., 8:99. (1922a) A study of Trypanosoma americanum. Ibid., 8:136. Grasse, P.-P. (1926) Contribution a l'etude des flagelles parasites. Arch. zool. exper. gen., 65:345. (1952) Traite de zoologie. I. Fasc. 1. Paris.

366

PROTOZOOLOGY
and Deflandre, G.
Grasse (1952),
p. 599.
:

(1952)

Ordre des Bicoecidea.

In:

Hardin, G.: (1942) An investigation of the physiological requirements of a pure culture of the heterotrophic flagellate, Oikomonas termo Kent. Physiol. Zool., 15:466. (1944) Physiological observations and their ecological significance: etc. Ecology, 25:192.

(1944a) Symbiosis of 304.

Paramecium and Oikomonas.

Ibid., 25:

Hartmann, M. and Noller, W.:

(1918) Untersuchungen ueber die Cytologic von Trypanosoma theileri. Arch. Protist., 38:355. Hegner, R. W. and Schumaker, E.: (1928) Some intestinal amoebae and flagellates from the chimpanzee, etc. J. Parasit., 15:31. Hofeneder, H. (1925) Ueber eine neue Caspedomonadine. Arch. Protist., 51:192. Hogue, Mary J.: (1933) A new variety of Retortamonas intestinalis from man. Am. J. Hyg., 18:433. (1936) Four races of Retortamonas intestinalis. Ibid., 23:80. Hollande, A.: (1936) Sur la cytologie d'un flagelle du genre Bodo. C. R. Soc. Biol., 123:651.' (1942) Etudes cytologique et biologique de quelques flagelles libres. Arch. zool. exper. gen., 83:1. (1952) Ordre des Bodonides. In: Grasse (1952), p. 669. Holmes, F. O.: (1924) Herpetomonad flagellates in the latex of milkweed in Maryland. Phytopathology, 14:146. (1925) The relation of Herpetomonas elmassiani to its plant and insect hosts. Biol. Bull., 49:323. Ivanic, M.: (1936) Zur Kenntnis der Entwicklungsgeschichte bei Mastigina hylae. Arch. Protist., 87:225.
:

Kirby, H. and Honigberg, B.: (1950) Intestinal flagellates from a wallaroo, Macropus robustus. Univ. California Publ. Zool., 55:
35.

Kozloff, E. N.: (1948) The morphology

of Cryptobia helicis. J. Morphol., 83:253. Kudo, R. R.: (1921) On some Protozoa parasitic in freshwater fishes of New York. J. Parasit., 7:166. (1923) Skate trypanosome from Woods Hole. Ibid., 9: 179. Lackey, J. B.: (1942) Two new flagellate Protozoa from the Tennessee River. Tr. Am. Micr. Soc, 61:36. Laird, M. (1951) Studies on the trypanosomes of New Zealand fish. Proc. Zool. Soc, London, 121:285. Lapage, G.: (1925) Notes on the choanoflagellate, Codosiga botrytis. Quart. J. Micr. Sc, 69:471. Laveran, A. and Mesnil, F.: (1901) Sur les flagelles a membrane ondulante des poissons, etc. C. R. Acad. Sc, 133:670. (1912) Trypanosomes et trypanosomiases. 2 ed.
:

Paris.
J.: (1846) Description of a new genus and species of Entozoa. Proc. Acad. Nat. Sc. Philadelphia, 3:100. Lemmermann, E.: (1914) Protomastiginae. Susswasserflora Deutschlands. H. 1.

Leidy,

PROTOMONADINA
Mavor,
:

367

J. W. (1915) On the occurrence of a trypanosome, probably Trypanoplasma borreli, etc. J. Parasit., 2:1. Minchin, E. A. and Thomson, J. D.: (1915) The rat trypanosome, Trypanosoma lewisi, in its relation to the rat flea, etc. Quart. J. Micr.Sc, 60:463. Nelson, R. (1922) The occurrence of Protozoa in plants affected with mosaic and related diseases. Tech. Bull. Bot. Stat. Michigan Agr. Coll., no. 58. Nie, D.: (1950) Morphology and taxonomy of the intestinal Proto:

zoa of the guinea-pig, Cavia porcella.

J.

Morphol., 86:381.

Nieschulz, O.: (1928) Zoologische Beitrage zum Surra problem. XVII. Arch. Protist., 61:92. Novy, F. G. and MacNeal, W. J.: (1905) On the trypanosomes of
birds. J. Infect. Dis., 2:256. of Chagas' disease in the State of Texas. Am. J. Trop. Med., 22:623. (1943) Infectivity of the Texas strain of Trypanosoma cruzi toman. Ibid., 23:309. (1950) The present status of Chagas' disease in the United States. Rev. Soc. Mexicana Hist. Nat., 10:91. Pascher, A.: (1925) Neue oder wenig bekannte Protisten. XVII. Arch. Protist., 51:549. (1929) XXI. Ibid., 65:426. (1943) Eine neue Art der farblosen Flagellatengattung Histiona aus den Uralpen. Ibid., 96:288. Reynolds, B. D.: (1927) Bicosoeca kepneri. Tr. Am. Micr. Soc, 46:54. (1934) Studies on monad flagellates. I, II. Arch. Protist., 81 399. Robertson, M.: (1911) Transmission of flagellates living in the blood of certain freshwater fishes. Philos. Trans., B, 202:29. Roskin, G. and Romanowa, K. (1928) Die Kernteilung bei Leishmania tropica. Arch. Protist., 60:482. and Schischliaiewa, S.: (1928) Die Kernteilung bei Trypanosomen. Ibid., 60:460. Roudabush, R. L. and Coatney, G. R. (1937) On some blood Protozoa of reptiles and amphibians. Tr. Am. Micr. Soc, 56:

Packchanian, A.: (1942) Reservoir hosts

291.

Scherffel, A.: (1924) Ueber die Cyste von Monas. Arch.

48:187.

Protist.,

Schindera, M.: (1922) Beitrage zur Biologie, Agglomeration und Ztichtung von Trypanoplasma helicis. Ibid., 45:200. Swaminath, C. S., Shortt, E. and Anderson, A. P.: (1942) Transmission of Indian kala-azar to man by the bites of Phlebotomus argentipes. Indian J. Med. Research, 30:473. Taliaferro, W. H.: (1921) Variation and inheritance in size in Trypanosoma lewisi. I. Proc Nat. Acad. Sc, 7:138. (1921a) II. Ibid., 7:163. (1923) A study of size and variability, throughout the course of "pure line" infections, with Trypanosoma lewisi. J. Exper. Zool., 37:127.

368

PROTOZOOLOGY
lewisi

to

A reaction product in infections with Trypanosoma which inhibits the reproduction of the trypanosomes. J. Exper. Med., 39:171. (1926) Variability and inheritance of size in Trypanosoma
(1924)
lewisi. J.

Exper. Zool., 43:429.

lewisi in rats

(1932) Trypanocidal

Trypanosoma

and reproduction-inhibiting antibodies and rabbits. Am. J. Hyg., 16:32.

(1938) Ablastic and trypanocidal antibodies against Trypanosoma duttoni. J. Immunol., 35:303. and Taliaferro, Lucy G.: (1934) Complement fixation, precipitin, adhesion, mercuric chloride and Wassermann tests in equine trypanosomiasis of Panama. Ibid., 26:193. Usinger, R. L.: (1944) The Triatominae of North and Central America and the West Indies and their public health signifi-

cance. U. S. Publ. Health Bull., no. 288. Vianna, G.: (1911) Sobre uma nova especie de Leishmania. Brazil Medico, no. 41. Weinstein, P. P. and Pratt, H. D.: (1948) The laboratory infection of Triatoma neotomae Neiva with Trypanosoma cruzi, etc.
J. Parasit.,

34:231.
(1932)

Wenrich, D. H.:

The

relation of the protozoan flagellate,

etc. Tr.

Retortamonas gryllotalpae,

Am.

Micr. Soc, 51:225.

Wenyon,

C. M.: (1911) Oriental sore in Bagdad, etc. Parasitology, 4:273. (1926) Protozoology. London and Baltimore. Wolcott, G. B.: (1952) Mitosis in Trypanosoma lewisi. J. Morphol.,

90:189.

Wood, Fae

Natural and experimental infection of Uhler and mammals in California with American human trypanosomiasis. Am. J. Trop. Med., 14:497. (1936) Trypanosoma neotomae sp. nov., etc. Univ. California Publ. Zool., 41:133. and Wood, S. F.: (1941) Present knowledge of the distribution of Trypanosoma cruzi in reservoir animals and vectors. Am. J. Trop. Med., 21:335. Yamasaki, S.: (1924) Ueber Leptomonas ctenocephali, etc. Arch. Protist,, 48:137.
D.:
(1934)

Triatoma protracta

Chapter

15

Order 3 Polymastigina Blochmann

Zoomastigina placed THE a dozen or more) family up
in this

to

flagella

group possess 3-8 (in one and generally speaking,

and structures. Many and one to many nuclei and the body is covered by a thin pellicle which allows the organism to change form, although each species shows a typical form. The cytoplasm does not show any special cortical differentiation; in many, there is an axial structure known as axostyle or axostylar filaments (p. 70). In Trichomonadiare minute forms with varied characters
possess a cytostome
dae, there
is usually a rod-like structure, known as costa (Kunstler), along the base of the undulating membrane and in Devescovinidae, there is a subtriangular body, the cresta, directly below the basal portion of the trailing flagellum, which in some species is very large

and capable of movement. At the time of division, the old costa is retained and a new one is formed; the cresta however is resorbed and two new ones are produced (Kirby). Parabasal bodies of various form and structure occur in many species.

The majority of Polymastigina inhabit the digestive tract of animals and nutrition is holozoic or saprozoic (parasitic). Many xylophagous forms hold symbiotic relationship with the host termites. Asexual reproduction is binary or multiple fission. Encystment is common. Sexual reproduction has been recognized in a few species.

Taxonomy

of species living in termites (Kirby, 1926).

With 1 nucleus With 2 nuclei With more than

2 nuclei

Suborder 1 Monomonadina Suborder 2 Diplomonadina (p. 392) Suborder 3 Polymonadina (p. 396)
I

Suborder

Monomonadina
(p.

Without axial organella Family 1 Trimastigidae With 3 flagella With 4 flagella None undulates on body surface Without cell-organ of attachment. Family 2 Tetramitidae Family 3 Streblomastigidae With rostellum One undulates on body surface Family 4 Chilomastigidae Family 5 Callimastigidae With more than 4 flagella With axial organella Without undulating membrane Without cresta Flagella not adhering to body Family 6 Polymastigidae Without rostellum Family 7 Oxymonadidae With rostellum
. .
.

370)

(p. (p.

(p.
(p.

371) 374) 374) 375)

(p. (p.

376) 378)

369

370
Flagellar cords on

PROTOZOOLOGY
body surface
Family S Dinenymphidae Family 9 Devescovinidae .Family 10 Trichomonadidae
(p. (p. (p.

With cresta With undulating membrane.

379) 380) 385)

Family

Trimastigidae Kent

Genus Trimastix Kent. Ovate or pyriform; naked; free-swimming; with a laterally produced membranous border; 3 flagella (1 anterior
flagellum vibrating, 2 trailing); salt water. Species (Grasse, 1952a).
T.

marina K.

(Fig. 154, a).

About

18ju long; salt

water.

Fig. 154. a, Trimastix marina,

X1250 (Kent);

b, Dallingeria drysdali,

X2000 (Kent);

c,

Macromaslix lapsa, X1500 (Stokes).

T. convexa Grasse (Coelotrichomastix convexa Hollande) (Fig. 167,

a).

In life 10-22/* by 8-10/x; dorsal side strongly convex, ventral side concave; three free flagella nearly equally long, fourth flagellum borders the undulating membrane, present on the concave side and becomes free beyond the posterior end of body; spherical nucleus voluminous, with a large endosome; free-living and coprozoic (Hollande, 1939; Grasse, 1952a).

Genus Dallingeria Kent. Free-Swimming or attached; with trailbody small; with drawn-out anterior end; fresh water with decomposed organic matter.
ing flagella;

D. drysdali K. (Fig. 154,

long stagnant water.
;

b).

Small; elongate oval; less than 6^

Genus Macromastix Stokes.

Free-swimming,

somewhat

like

POLYMASTIGINA
Dallingeria,
terior end;

371

but anterior region not constricted; 3 flagella from anone contractile vacuole; fresh water. M. lapsa S. (Fig. 154, c). Ovoid; 5.5/x long; anterior flagellum 1/2 and trailing flagella 2-3 times body length; pond water. Genus Mixotricha Sutherland. Large; elongate; anterior tip spirally twisted and motile; body surface with a coat of flagella in closely packed transverse bands (insertion and movement entirely different from those of Trichonympha) except posterior end 3 short flagella at anterior end; nucleus, 20m by 2ju, connected with blepharoplasts by prolonged tube which encloses nucleus itself; cytoplasm
;

with scattered wood chips; in termite gut. One species. Taxonomic

position undetermined.

M. paradoxa
of

S. About 340^ long, 200> broad and 25/x thick in gut Mastotermes darwiniensis ; Australia (Sutherland).
;

Family 2 Tetramitidae Butschli

Genus Tetramitus Perty.

Ellipsoidal or pyriform; free-swimming;

flagella

cytostome at anterior end; 4

1936).

unequal in length; a contractile

vacuole; holozoic; fresh or salt water or parasitic. Species (Klug,

T. rostratus P. (Fig. 15G, a). Body form variable, usually ovoid and narrowed posteriorly: 18-30ju by 8-11 n; stagnant water. Bunting (1922, 1926) observed an interesting life cycle of what appeared to be this organism which she had found in cultures of the caecal content of rats (Fig. 155). Nuclear division (Bunting and Wenrich, 1929). T. pyriformis Klebs (Fig. 156, b). Pyriform, with pointed posterior end; 11-13/x

by 10-1 2/x; stagnant

c).

water.

T. salinus (Entz) (Fig. 156,

flagella;

2 anterior flagella, 2 long trailing

posterior end; cytopharynx temporary

nucleus anterior; cytostome anterior to nucleus; a groove to and length variable; 20-30^
it

long (Entz); 15-19ju long (Kirby). Kirby observed

in a pool with

a high salinity at Marina, California. Genus Collodictyon Carter. Body highly plastic; with longitudinal
furrows; posterior end bluntly narrowed or lobed; no apparent

cytostome; 4

flagella; a contractile

vacuole anterior; fresh water.

C. triciliatum C. (Fig. 156, d). Spherical, ovoid or heart-shaped;

27-60/x long; flagella as long as the body;

pond water. Cytology

(Rhodes, 1919); food ingestion (Belaf, 1921). Genus Costia Leclerque. Ovoid in front view, pyriform in profile; toward the right side, there is a shallow depression which leads into

cytostome

(?)

and from which extend two long and two short

in

flagella

(only two flagella (Andai, 1933)); contractile vacuole posterior; en-

cystment ectoparasitic
;

freshwater

fishes.

372

PROTOZOOLOGY

Fig. 155. Diagram illustrating the life-cycle of Tetramitus rostratus (Bunting), a, cyst; b, vegetative amoeba; c, division; d, after division; e, f, stages in transformation to flagellate form; g, fully formed flagellate; h, flagellate prior to division; i, flagellate after division; j-1, trans-

formation stages to amoeba.

C. necatrix

(Henneguy)
fj.

(Fig. 156, e-j). 10-20ju

by
;

5-10/x (Henne-

guy), 5-18/x by 2.5-7 (Tavolga and Nigrelli, 1947) nucleus central; uninucleate cyst, spherical, 7-10/iin diameter; when present in large numbers, the epidermis of the fish appears to be covered by a whitish
coat.

by 5-8 m, on

Davis (1943) found a similar organism which measured 9-14^ trout, Salmo irideus and Salvelinus fontinalis, and
it

named

Costia pyriformis.

Genus Enteromonas da Fonseca (Tricercomonas Wenyon and

O'Connor). Spherical or pyriform, though plastic; 3 anterior flagella; the fourth flagellum runs along the flattened body surface and extends a little freely at the posterior tip of body; nucleus anterior; no cytostome; cyst ovoid and with 4 nuclei when mature; parasitic

POLYMASTIGINA
in

373

mammals, da Fonseca (1915) originally observed only 3 flagella and no cysts; 4 flagella and encysted forms were noticed in Tricercomonas by Wenyon and O'Connor (1917); in da Fonseca's original preparations, Dobell (1935) observed 4 flagella as well as cysts

and concluded that Enteromonas and Tricercomonas are one and the same flagellate.

formis,

a, Tetramitus rostratus, X620 (Lemmermann); b, T. pyriX670 (Klebs); c. T. salinus, X1630 (Kirby); d, Collodictyon triciliatum, X400 (Carter); e-j, Costia necatrix (e, f, XSOO (Weltner); g-i, X1400 (Moroff); j, two individuals attached to host integument X500 (Kudo)); k, Enteromonas hominis, X1730 (Wenyon and O'Connor); 1, Copromastix prowazeki, X1070 (Aragao).

Fig. 156.

E. hominis da F. (T. intestinalis W. and O) (Figs. 156, k; 157, ad). Trophozoites 4-l(hz by 3-6ju; nucleus circular or pyriform, with a
large endosome, near anterior end; 4 flagella take their origins in

blepharoplasts located close to nucleus; cytoplasm vacuolated or

reticulated, contains bacteria; cysts ovoid, 6-8/x

by

4-6/z;

with

1, 2,

or 4 nuclei; commensal in the lumen of

diarrhoeic stools. Widely distributed.

human

intestine;

found

in

slightly smaller; in the

E. caviae Lynch. Similar to the species mentioned above, but caecum of guinea-pigs (Lynch, 1922). Cytol-

ogy (Nie, 1950).

374

PROTOZOOLOGY

'

Genus Copromastix Aragao. Four anterior flagella equally long; body triangular or pyramidal; coprozoic. C. prowazeki A. (Fig. 156, I). About 16-18/* long; in human and
rat faeces.

Genus Karotomorpha Travis (Tetramastix

pyriform; body more or
terior end, in
less rigid;

Alexeieff).

Elongate

four unequal flagella at the an-

two groups; nucleus anterior; without cytostome; Amphibia. Species (Travis, 1934). K. bufonis (Dobell) (Fig. 157, e). Spindle in shape; 12-16/x by 2-6/*; in the intestine of frogs and toads. Cytology (Grasse, 1926).
parasitic in the intestine of

Family 3 Streblomastigidae Kofoid and Swezy

Genus Streblomastix K. and

the anterior tip of which
is

S.

Spindle-form; with a rostellum,

enlarged into a sucker-like cup; below the

cup are inserted 4 (Kidder) or 6 (Kofoid and Swezy) equally long flagella; extremely elongate nucleus below rostellum; body surface with 4 or more spiral ridges; in termite gut. One species. S. strix K. and S. (Fig. 157, /, g). 15-52/* by 2-15/*; 4-8 spiral
ridges; blepharoplast in rostellum; in Termopsis angasticollis.

Family 4 Chilomastigidae Wenyon

Four flagella, one of which undulates in the cytostome. Genus Chilomastix Alexeieff. Pyriform; with a large cytostomal
cleft at anterior

end; nucleus anterior; 3 anteriorly directed flagella;

short fourth flagellum undulates within the cleft; cysts

intestine of vertebrates. Several species.

common;

in

C. mesnili (Wenyon) (Fig. 157, h-k). The trophozoite is oval or pyriform; 5-20 (10-15)/* long; jerky movements; a large cytosto-

mal

cleft

near anterior end; nucleus, vesicular, often without endoflagella

some; 3 anterior

short, undulates in the cleft

about 7-10/z long; the fourth flagellum which ridge is marked by 2 fibrils. The cyst pyriform; 7-10/* long; a single nucleus; 2 cytostomal fibrils and a short flagellum; commensal in the caecum and colon (some consider also in small intestine) of man. Both trophozoites and cysts occur in diarrhoeic faeces. It is widely distributed and very common. Cytology (Kofoid and Swezy, 1920); cultivation (Boeck, 1921). C. intestinalis Kuczynski. In guinea-pigs; 13-27/* by 51 1/x (Gei-

man, 1935);
C. cuniculi

8.8-28/*

C. bettencourti

by 6.6-11/* (Nie, 1950). da Fonseca. In rats and mice.

rabbits.

da F. In

C. caprae d. F. In goat.

POLYMASTIGINA

375

Fig. 157. a-d, Enteromonas hominis, XI 730 (Wenyon and O'Connor) b, living and c, stained trophozoites; d, a stained cyst); e, Karotomorpha bufonis, X2000 (Grass6); f, Streblomastix strix, X1030; g, anterior end of the organism, showing the rostellum, blepharoplast, sucking cup and flagella (Kidder); h-k, Chilomastix mesnili, X1530 (h, living and i, stained trophozoites; j, a fresh cyst; k, a stained cyst); 1, a stained trophozoite, and m, a stained cyst of C. gallinarum, X1330 (Boeck and Tanabe); n, Callimastix frontalis, XI 500 (Braune); o, C. equi, XI 100 (Hsiung).
(a,

C. gallinarum

Martin and Robertson

(Fig. 157,

I,

m). 11-20/x by

5-6^; in the caeca of turkeys and chicks. Morphology (Boeck and

Tanabe, 1926).

Family 5 Callimastigidae da Fonseca

Flagella 12 or more; in

stomach

of ruminants or in

caecum and

colon of horse.

Genus Callimastix Weissenberg. Ovoid; compact nucleus central

or anterior; 12-15 long flagella near anterior end, vibrate in unison.

Weissenberg (1912) considered this genus to be related to Lopho(p. 407), but organism lacks axial organellae;in Cyclops and alimentary canal of ruminants and horse. C. cyclopis W. In body-cavity of Cyclops sp. C. frontalis Braune (Fig. 157, n). 12 flagella; about 12ju long; flagella 30ju long; in cattle, sheep and goats.

monas

376
C. equi

PROTOZOOLOGY
Hsiung
(Fig.

157, o). 12-15 flagella; 12-18/*

by

7-10/*;

nucleus central; in caecum and colon of horse.

Family 6 Polymastigidae

Biitschli

Genus Polymastix

Biitschli.

Pyriform; four flagella arise from two

blepharoplasts located at anterior end; cytostome and axostyle in-

conspicuous; body often covered by a protophytan; commensals in

insects. Species (Grasse, 1926, 1952).

P. melolonthae (Grassi) (Fig. 158,

a). 1015/*
:

by
in

4-8/*;

body cov-

ered by Fusiformis melolonthae (Grasse, 1926)

the intestine of
etc.

Melolontha, Oryctes, Cetonia, Rhizotrogus, Tipula,

a, Polymastix melolonthae, X2000 (Grasse); b, Eutrichomastix X1450 (Kofoid and Swezy); c, E. batrachorum, X1350 (Dobell); d, E. axostylis, X2000 (Kirby); e, Chilomitus caviae (Nie); f, Hexamastix termopsidis, X2670 (Kirby); g, H. batrachorum; h, Protrichomonas legeri, Monocercomonoides melolonthae, X2000 (Grasse); j, X1000 (Alexeieff); Cochlosoma rostraturn, X1465 (Kiiriura).

Fig. 158.

serpentis,

i,

Genus Eutrichomastix Kofoid and Swezy (Trichomastix Blochmann). Pyriform; anterior end rounded; cytostome and nucleus anterior; 3 flagella of equal length arise from anterior end, the fourth trailing; axostyle projects beyond posterior end of body; all endocommensals.
E. serpentis (Dobell) (Fig. 158,
b).

About

10-25/* long; in intestine

POLYMASTIGINA
1915).

377

of snakes: Pituophis, Eutaenia, and Python (Kofoid and Swezy,

E. balrachorum (Dobell)
intestine of

(Fig.

158,

c).

Ovoid; 6-20/x long; in

Ranafusca (Dobell, E. axostylis Kirby (Fig. 158,

1909).
d).

Elongate, ellipsoid, or pyriform;

axostyle projecting; 5-10.5/xby 2-3.5/*; 3 anterior flagella 5-1 0/x long;

in

gut of Nasutitermes kirbyi (Kirby, 1931).

Genus Chilomitus da Fonseca. Elongate

veloped;
aboral
surface

oval; pellicle well de-

convex;

cytostome near anterior end,

through which four flagella originating in a bi-lobed blepharoplast, protrude; rudimentary axostyle; nucleus and parabasal body below the cytostome (da Fonseca, 1915). C. caviae da F. (Fig. 158, e). In the caecum of guinea-pigs; stained trophozoites 6-14/i by 3.1-4.6/x; cytoplasm contains siderophilic
bodies of

unknown nature
flagella, of

(Nie, 1950).

Genus Hexamastix
but with 6
basal

Alexeieff.

Body
trails;

similar to

Eatrichomastix,

which one

axostyle conspicuous; para-

body prominent. H. termopsidis Kirby (Fig. 158, /). Ovoidal or pyriform; 5-1 1m long; flagella 15-25^ long; in gut of Zootermopsis angusticollis and
H. caviae and H. robustus were described by Nie (1950) from the caecum of guinea-pigs.
H. balrachorum Alexeieff (Fig. 158, g). Oval or spindle form; 8-14ju by 4-8ju; flagella about body length; in gut of Triton taeniatus. Genus Protrichomonas Alexeieff. 3 anterior flagella of equal length, arising from a blepharoplast located at anterior end; parasitic.

Z. nevadensis; California (Kirby, 1930).

P. legeri A. (Fig. 158, h). In oesophagus of the marine

boops.

fish,

Box

Genus Monocercomonoides Travis (Monocercomonas

Grassi).

Small; 4 flagella inserted in pairs in two places; two directed anteriorly and the other two posteriorly; axostyle filamentous; parasitic.

Taxonomy

(Travis, 1932).
?').

M.

melolonthae (Grassi) (Fig. 158,

Ovoid: 4-1 5/x long;

in

the

larvae of Melolontha melolontha, etc.

Genus Cochlosoma Kotlan. Body

small, oval; sucker in the an-

terior half; 6 flagella; axostyle filamentous; parasitic (Kotlan, 1923).

C. rostratum Kimura (Fig. 158, j). In the colon of domestic ducks, Anas platyrhynchus and Carina moschata; 6-10m by 4-6. 5^ (Kimura, 1934). McNeil and Hinshaw (1942) observed this organism in the intestine of young poults and in the region of caecal tonsil in adults.

378

PROTOZOOLOGY
Family 7 Oxymonadidae Kirby

Genus Oxymonas

Janicki. Attached phase with a conspicuous

rostellum, the anterior end of which forms a sucking-cup for attach-

ment; pyriform. In motile phase, rostellum

rise to 2 flagella

is less

conspicuous; 2

blepharoplasts located near the anterior extremity of axostyle, give

each; axostyle conspicuous; xylophagous; in termite
in

and woodroach; sexual reproduction

some (Cleveland,

1950).

Fig. 159.
b,

a, b, Oxymonas dimorpha (Connell) (a, a motile form, X900; an attached aflagellate form, X460); c, 0. grandis, X265 (Cleveland);

d, Proboscidiella kofoidi,

X600

(Kirby).

0. dimorpha Connell (Fig. 159, a, b). Subovoid; delicate pellicle; axostyle slightly protruding; a pair of long anterior flagella from

2 blepharoplasts, connected

by

rhizoplast; nucleus anterior.

When

attached to intestine, rostellum elongate, flagella disappear; 17m by 14/z to 195/x by 165m; in Neotermes simplicicornis; California and

Arizona (Connell, 1930). 0. grandis Cleveland (Fig. 159,

c). Body 76m by 31m to 183m by 79m; rostellum varies 30-200m in length; nucleus without an endo-

POLYMASTIGINA

379

some, anterior, about 20-23/x in diameter; axostyle consists of a staining part and a non-staining part; in the intestine of Neotermes dalbergiae and N. tectonae (Cleveland, 1935). Genus Proboscidiella Kofoid and Swezy (Microrhopalodina Grassi and Foa; Kirbyella Zeliff). Attached and motile forms similar to Oxy-

monas; but multinucleate; 4

flagella

from each karyomastigont

Zeliff,

(p.

315); rostellum with filaments which extend posteriorly as axostyles; in termite gut (Kofoid

and Swezy, 1926;

1930a).

P. kofoidi Kirby (Fig. 159, d). Average size 66m by 46m; rostellum as long as, or longer than, the body; karyomastigonts 2-19 or more

(average 8) each mastigont with 2 blepharoplasts from which extend 4 flagella; in Cryptolermes dudleyi (Kirby, 1928).
;

Family 8 Dinenymphidae Grassi and Foa

Genus Dinenympha Leidy. Medium large; spindle form; 4-8 adhering to body which are spirally twisted about one turn; the flagella free at the posterior end; axostyle varies from cord to band; pyriform nucleus, anterior, with a large endosome; in terflagellar cords

mite gut. Species (Koidzumi, 1921). D. gracilis L. (Fig. 160, a). 24-50/1 by 6-1 2m body flattened and twisted; ends attenuated; with adhering protophytes; in Reticuli;

termes flavipes.

D. fimbriata Kirby

(Fig. 140, b).

52-64m by 8-18/x; 4-8

flagellar

cords; with adherent protophytes; axostyle varies in width; in

Reticuliterm.es hesperus (Kirby, 1924).

Genus Pyrsonympha Leidy. Large; club-shaped, the posterior end rounded; body surface with 4-8 flagellar cords which are arranged lengthwise or slightly spirally; flagella extend freely posteriorly; blepharoplast at the anterior tip, often with a short process for attachment; axostyle a narrow band, may be divided into parts; large pyriform nucleus anterior; in termite gut. Species (Koidzumi, 1921)
is

nuclear division (Cleveland, 1938).

P. vertens L. (Fig. 160,
1925).
c).

cords; in Reticulitermes flavipes. Cytology

About 100-150m long; 4-8 flagellar (Duboscq and Grasse,

P. granulata Powell (Fig. 160, d). 40-120m by 5-35m; 4-8 flagellar

cords; in Reticulitermes hesperus (Powell, 1928).

Genus Saccinobaculus Cleveland. Elongate to spherical; 4, 8, or and project out freely; axostyle is an extremely large paddle-like body and undulates, serving as cellorgan of locomotion; posterior end of axostyle enclosed in a sheath; in woodroach gut.
12 flagella adhere to the body,

380
S.

PROTOZOOLOGY
ambloaxostylus C. (Fig.
160,
e-g).

65-1 10/x by 18-26/*; in

Cryptocercus punctulatus. Sexual reproduction (Cleveland, 1950a).

Genus Notila Cleveland. Body elongate, plastic; four flagella, the attached portion of which shows attached granules (Fig. 160, i); axostyle large, paddle-like, much broader than that of Pyrsonympha

a, Dinenympha gracilis, X730;b, D. fimbriate/,, X625 (Kirby); Pyrsonympha vertens, X730; d, P. granulata, X500 (Powell); e-g, Saccinobaculus ambloaxostylus (Cleveland) (e, whole organism, X600; f, anterior and g, posterior portion of vegetative individual); h-j, Notila anterior and j, posproteus (Cleveland) (h, diploid individual, X360;

Fig. 160.

c,

i,

terior

ends of the organism).

no axostyler sheath at posterior end, but with large granules or

spherules

embedded

in it; in Cryptocercus punctulatus.

N. proteus C.

(Fig. 160, h-j). Size not given;

gametogenesis and
of the host; diploid

sexual fusion, induced

number

of

by the molting hormone chromosomes 28 (Cleveland, 19501)).

Family 9 Devescovinidae Doflein

Usually 3 anterior flagella and a trailing stout flagellum; near base of trailing flagellum an elongated cresta (becoming a large

POLYMASTIGINA
internal

381

membrane

lightly adheres to

in some species) (Fig. 161); trailing flagellum body surface along edge of cresta; axostyle; para-

basal
lating

body of various forms; single nucleus anterior; without undumembrane; generally xylophagous. Cytology and morpho-

genesis (Kirby, 1944).

papilla
ant. flagella ant. lamella

bleph. group
nucl. rhiz.

parab.

fil.

parab. body

cresta

chrom. mass
nucl.

memb.

chr. cone in ax.

parab. spiral

chromoph. element
of pb.
axostyle

tr.

flagellum

Fig. 161.

niscata,

diagrammatic view of the anterior part of Devescovina lemshowing the cresta and other organellae (Kirby).

Genus Devescovina Foa. Elongate body, usually pointed posteabout the body length; trailing flagellum, slender to band-form, about 1-1.5 times the body length; cresta; parabasal body spiraled around axostyle or nucleus; in termite inriorly; 3 anterior flagella

testine.

Many species

(Kirby, 1941, 1949).

D. lemniscata Kirby (Figs. 161; 162, a). 21-51/* by 9-17//; trailing flagellum a band; cresta long, 7-9/*; in Cryptotermes hermsi and many species of the genus; species of Neotermes, Glyptotermes and Kalotermes (Kirby, 1926a). Genus Parajoenia Janicki. Medium large; with rounded extremities;

3 anterior flagella

and

trailing flagellum long; cresta of

moder-

ate size; parabasal

body

well developed with its anterior end close to

blepharoplast;
P. grassii

stout axostyle

expanded anteriorly into

leaf -like

capitulum, bearing a longitudinal keel; in intestine of termites.

J. (Fig.

162, b). 29-59/*

by

12-33/*; trailing flagellum

382

PROTOZOOLOGY

Fig. 162. a, Devescovina lemniscata, X1600; b, Parajoenia grassii, with attached spirochaetes, XH50; c, Foaina nana, XH50; d, Macrotrichomonas pulchra, X1600 (all after Kirby); e, Metadevescovina debilis, X1130
(Light, modified).

POLYMASTIGINA
stout, cordlike; cresta

383

about

9/t

long; in Neotermes connexus (Kirby,

1937, 1942a).

Genus Foaina Janicki {Janickiella Duboscq and Grasse; ParaCrucinympha Kirby). Small to medium large; 3 anterior flagella; trailing flagellum about twice the body length; cresta slender, 2.5-17/x long; parabasal body single, in some with rami; in
devescovina,

intestine of termites.

Many species (Kirby,

1942a, 1949).

by 4.5-8.5/x; trailing flagellum a moderately stout cord, 2-3 times the body length; cresta slender, 8.5m long; filament part of the parabasal body reaching the middle
F.

nana Kirby

(Fig. 162, c). 6-18/x

of body; in Cryptotermes hermsi

species of Glyptotermes, Rugitermes,

and many species of the genus; also and Procryptotermes (Kirby,

1942a).

Genus Macrotrichomonas

Grassi. Large; 3 anterior flagella; trail-

ing flagellum well developed, 1-1.5 times the

body

length; cresta a

broad internal membrane, 21-86/i long; parabasal body coiled around

the axostyle, 1-13 times; in termite gut. Several species (Kirby,
1942, 1949).

M. pulchra G. (Fig. 162, d). 44-91/x by 21-41/*; trailing flagellum band-form; cresta large; parabasal body coiled closely 4-10 times; in Glyptotermes parvulus, and many other species of the genus (Kirby,
1942).

Genus Metadevescovina Light. Moderately

flagella;

large;

anterior

a short trailing flagellum; cresta small; parabasal

body

loosely coiled

around axostyle; anterior end of axostyle

in a loop;

in termite gut.

Many

species (Light, 1926; Kirby, 1945).

debilis L. (Fig. 162, e). 30-70/*

by

15-30/*; in Kalotermes hub-

bardi.

Genus Caduceia Franca. Large; 3 long anterior

long; parabasal

flagella; trailing

flagellum slender, shorter than body; cresta relatively small, 1 12/z

body

coiled

around axcstyle 2-20 times; nucleus

relatively large; axostyle terminates in filament; in termites. Several

species (Kirby, 1942, 1949).

C. bugnioni

Kirby

(Fig. 163, a). 48-80/*

by

18-40/*; in Neotermes

greeni (Kirby, 1942).

Genus Hyperdevescovina Kirby. Similar to Caduceia; but cresta very small ;stout axostyle projects from the body in Proglyptotermes, Neotermes; New Zealand and South Africa. Many species (Kirby,
;

1949).

H.

calotermitis (Nurse). 52-1 14/*

by

30-65//; projecting portion of

the axostyle 45-63/*; in Proglyptotermes browni;

New

Zealand.
anterior

Genus Pseudodevescovina Sutherland. Large; 3 short

384
fiagella;

PROTOZOOLOGY
one short
trailing flagellum; axostyle stout; cresta of

moder-

ate size; parabasal

body

large, divided into a

number

of attached

cords; in termite gut. Several species (Kirby, 1945).

P. uniflagellate, S. (Fig. 163,

fiagella, 30/z long; trailing

b).

52-95m by 26-60/z; 3 delicate

little

flagellum a

stouter; cresta 11-20/*

long;

main parabasal body C-shaped, with 7-19 attached

cords; in

Kalotermcs insularis (Kirby, 1936, 1945).

lata,

a, Caduceia bugnioni, X930; b, Pseudodevescovina unifiagelX1190; c, Bullanympha silvestrii, X780 (all after Kirby); d, e, Gigantomonas herculea (Dogiel) (d, X530; e, amoeboid phase (Myxo-

Fig. 163.

monas), X400).

POLYMASTIGINA
Genus Bullanympha Kirby. Flagella and
part of parabasal

385

cresta similar to those in

Pseudodevescovina; axostyle similar to that in Caduceia; proximal

body bent

in

U-form around the nucleus and

at-

tached voluminous distal portion coiled around the axostyle; in

termite gut (Kirby, 1938, 1949). B. silvestrii K. (Fig. 163, c). 50-138/*
long; distal portion of parabasal

by 35-100/*; cresta about 5.8m body coils around axostyle about

twice; in Neotermes erythraeus.

Genus Gigantomonas Dogiel (Myxomoiias D.). Medium large; 3 and stout trailing flagellum; cresta conspicuously large; large axostyle; in termite gut. According to Kirby (1946),
anterior flagella; a long

membrane is a large cresta; in aflagellate phase (Myxomonas) the nuclear division takes place. G. herculea D. (M. polymorpha D.) (Fig. 163, d, e). 60-75/* by 30-35/z; in the intestine of Hodotermes mossambicus (Kirby, 1946).
the so-called undulating

Family 10 Trichomonadidae Wenyon

Kirby (1947) considers that Trichomonas and allied genera should be grouped in a new order Trichomonadina. He proposes four families: Monocercomonadidae, Devescovinidae, Calonymphidae and Trichomonadidae to be placed under it. Morphology and taxonomy
(Grasse, 1952a}.

Genus Trichomonas Donne. Pyriform

ing

typically with four free an-

terior flagella; fifth flagellum along the outer

margin

of the undulat-

membrane; costa

at the base of the

membrane; axostyle de-

veloped, often protruding beyond the posterior end of the body; encystment has not been definitely observed; all parasitic. Numerous species (Wenrich, 1944). Cytology and morphogenesis (Kirby, 1944)
division process (Kuczynski, 1918).
T. hominis (Davaine) (Fig. 164, a). Active flagellate, undergoing a

jerky or spinning movement; highly plastic, but usually ovoid or

pyriform; 5-20/t long; cytostome near anterior end; 4 anterior

flagella equally lpng; fifth flagellum

which

is

seen in

life

in degenerating individuals the

undulate, even after loss of flagella,

bacteria;

membrane membrane may simulating amoeboid movement;

borders undulating

axostyle straight along the median line; vacuolated cytoplasm with

hoeic stools. Wenrich (1944) states that in

and ileum of man; found in diarrall 20 cases which he studied, some or most of the individuals showed five anterior flagella and two unequal blepharoplasts. Since encysted forms have not yet been found, transmission is assumed to be carried on by trophozoites. According to Dobell (1934),

commensal

in the colon

386

PROTOZOOLOGY

he became infected by an intestinal Trichomonas of a monkey (Macacas nemestrinus) by swallowing "a rich two-day culture" plus bacteria which were mixed with 10 cc. of sterilized milk on an empty stomach. The presence of Trichomonas in his stools was established

on the 6th day by culture and on the 13th day by microscopical examination after taking in the cultures. The infection which lasted for about four and a half years, did not cause any ill effects upon

Fig.
in

164. Diagrams showing the species of Trichomonas which live man, X2500 (modified after Wenrich). a, Trichomonas hominis; b, T.
c.

tenax;

T. vaginalis.
is

him.

The organism
at

killed after five minutes'

exposure to

N/20

37C, but at 15-22C, is able to survive, though in small numbers, up to 15 minutes after exposure to the acid (Bishop, 1930). This flagellate is widely distributed and of common occurrence, especially in tropical and subtropical regions. T. tenax (Miiller) (T. elongata Steinberg; T. buccalis Goodey) (Fig. 164, b). Similar to the last mentioned species; commensal in the tartar and gum of human mouth. Nomenclature (Dobell, 1939). T. vaginalis Donne (Fig. 164, c). Broadly pyriform; 10-30/x by 10-20/x; cytoplasm contains many granules and bacteria; cytostome inconspicuous; nutrition parasitic and holozoic; parasitic in human reproductive organ. Although the organism does not enter the vagi-

HC1

nal tissues,

many

observers believe

it

to be responsible for certain

it

diseases of the vagina. Trussell

and Johnson (1945) maintain that

POLYMASTIGINA
is

387

membrane and according

capable of inciting an inflammatory reaction in the vaginal mucous to Hogue (1943), this flagellate produces a
cells in tissue culture. It

substance which injures the

occurs also in

the male urethra (Feo, 1944). Morphology (Reuling, 1921; Wenrich, 1939, 1944, 1944a, 1947); taxonomy, structure and division (Hawes,
1947); comprehensive

monograph

(Trussell, 1947).

Because of the morphological similarity of these three species of

Fig. 165.
T. gallinae,
d,

Trichomonas microti, X2000 (Wenrich and Saxe); b-d, (Stabler) (b, from domestic pigeon; c, from turkey; from red- tailed hawk); e, T. linearis, X2000 (Kirby).
a,

X1765

human Trichomonas,

number

of workers maintain that they

may

be one and the same species. Dobell (1934) inoculated a rich culture of Trichomonas obtained from his stools into the vagina of a monkey

(Macacus rhesus) and obtained a positive infection which was easily proven by culture, but unsatisfactorily by microscopical examination of smears. The infection thus produced lasted over three years and did not bring about any ill effect on the monkey. He considers that T. vaginalis and T. hominis are synonyms and that there occur diverse strains different in minor morphological characters and physiological properties. Andrews (1929) noted the organism obtained from vaginal secretion was larger than T. hominis and its undulating membrane extended for 1/2 or 2/3 the body length, but when cultured in vitro, the organisms became smaller in size and the undulating membrane protruded beyond the body as a free flagellum. On the other hand, Stabler and his co-workers (1941, 1942) failed to obtain infections in volunteers

by inoculating intravaginally with

cul-

388
tures of T. hominis.
of

PROTOZOOLOGY
Wenrich (1944) who made comparative studies
considers that there exist distinctly recog-

human Trichomonas,

nizable morphological differences

among

the three

human

species of

Trichomonas, as shown in Fig. 164. T. macacovaginae Hegner and Ratcliffe. In the vagina of Macacus rhesus. Dobell (1934) held that this is identical with T. vaginalis and
T. hominis.
T. microti

Wenrich and Saxe

(Fig. 165, a). In the

caecum

of ro-

dents, Microtus pennsylvanicus, Peromyscus leucopus, Rattus norvegicus, Mesocricetus auratus;

4-9 m long; four free

flagella;

a blepha-

roplast; undulating

membrane medium

long; axostyle conspicuous.

and Delprato) (Fig. by 2-9m; ovoid nucleus anterior together with a blepharoplast and parabasal body axostyle protrudes a little
T. gallinae (Rivolta) (T. columbae Rivolta
165, b-d). Pyriform; 6 19>u
;

cytoplasmic granules; four anterior flagella 8-13/x long; autotomy; in the upper digestive tract of pigeon and also turkey, chicken, and dove. Experimentally it is transferable to quail, bob-white, hawk,
canary,
etc.,

and often

fatal to hosts. Species (Travis, 1932a).

Mor-

phology (Stabler, 1941); pathology (Levine and Brandly, 1940);

transmission (Levine
bler, 1951).
et al.,

1941); distribution (Barnes, 1951; Sta-

T. linearis

Kirby

(Fig. 165, e).

3-8 n;

in the intestine of Orlhognathotermes wheeleri;

Elongate spindle in form; 9-24^ by Panama. Other

species in termites (Kirby, 1931).

T. limacis (Dujardin). In the intestine

and liver-tubules

of slugs,

Deroceras agreste (Dujardin, 1841) and

Limax flavus

(Kozloff, 1945);

subspherical to ellipsoidal; 11-17/x by 8-13m; four anterior flagella; undulating membrane extends to posterior end, with free flagellum
(Kozloff).

Genus Tritrichomonas Kofoid. Similar

parasitic.

to Trichomonas in appear-

ance, behavior and structure, but with only three anterior flagella;

Many

species.

T. foetus (Riedmuller) (Fig. 166, a, b). In the genitalia of cattle;

pathogenic; 10-15/z long; transmission by sexual act, from cow to bull or bull to cow and also by "natural contamination" (Andrews
Miller, 1936) from cow to cow. Infection brings about permanent or temporary suspension of the conception or the death of foetus. Sheep is susceptible (Andrews and Rees, 1936). Morphology (Wenrich and Emmerson, 1933; Morgan and Noland, 1943; Kirby, 1951); effect on tissue culture (Hogue, 1938); effect on reproducti-

and

bility of

cow

(Bartlett, 1947, 1948).

T. fecalis Cleveland.

5m by

4ju

to 12/x

by

6m; average dimensions

POLYMASTIGINA
8.5/i

3S9

by

5.7^; axostyle long, protruding 1/3-1/2 the

body length

from the posterior end; of 3 flagella, one is longer and less active than the other two; in the faeces of man. Its remarkable adaptability observed by Cleveland was noted elsewhere (p. 34).

Fig. 166. a, Tritrichomonas foetus in life, X1330 (Morgan and Noland); stained T. foetus, X1765 (Wenrich and Emmerson); c, d, T. muris, X2000 (Wenrich); e, T. batrachorum, X1465 (Bishop); f, g, T. augusta, X 1455 (Samuels) h, T. brevicollis, X2000 (Kirby) i, j, Pseudotrichomonas keilini, X2200 (Bishop).
h, a
; ;

Fusiform; 10-16/* by 5-10/*; 3 beyond body; axostyle large, its tip protruding; in the caecum and colon of mice (Mus, Peromyscus) (Wenrich, 1921) and ground squirrel (Citellus lateralis chrysodeirus) (Kirby and Honigberg, 1949). The organism
T. muris (Grassi) (Fig. 166,
c,

d).

anterior flagella short, posterior flagellum extends

390

PROTOZOOLOGY

has been found within nematodes which coinhabit the host intestine. For example, Theiler and Farber (1932) found the flagellate in the chyle-stomach of Aspicularis tetraptera and Syphacia obvelata, and

Becker (1933) noted two active individuals of this flagellate within the egg shell of the last-named nematode. Morphology and division
(Kofoid and Swezy, 1915; Wenrich, 1921). T. caviae (Davaine). Ovoid or pyriform; 5-22/z long; undulating

membrane long; axostyle protrudes; spherical cysts about 7 m in diameter (Galli-Valerio, 1903; Wenyon, 1926). Cytology and reproduction (Grasse and Faure, 1939). T. batrachorum (Perty) (Fig. 166, e). Ovoid; 14-18/* by 6-10/x (Alexeieff); in culture, 7-22/z by 4-7 ju (Bishop, 1931) axostyle without granules; in the colon of frogs and toads. Bishop (1934) succeeded in infecting the tadpoles of Rana temporaria and Bufo vulgaris by feeding them on cultures free from cysts. T. augusta Alexeieff (Fig. 166, /, g). Elongate spindle; 15-27/x by 5-13/z; thick axostyle protrudes, and contains dark-staining granules; in the colon of frogs and toads. Morphology and division (Kofoid and Swezy, 1915; Samuels, 1941); viability (Rosenberg, 1936); in frog liver lesions (Stabler and Pennypacker, 1939). T. brevicollis Kirby (Fig. 166, h). Ovoid, undulating membrane curved around end; 10-1 7m by 4-8m; in the intestine of Kalotermes
;

Panama. Genus Pseudotrichomonas Bishop. Body form, structure and movement, are exactly like those of Tritrichomonas, but free-living in freshwater pond (Bishop, 1939). P. keilini B. (Fig. 166, i, j). When alive 7-11m by 3-6m; highly plastic; young cultures contain more globular forms, while old cultures more elongated organisms; three unequally long anterior flagella; undulating membrane short, does not extend more than 1/2 the body and without a free flagellum; cytostome; holozoic, feeding
brevicollis;

on bacteria; nucleus anterior; axostyle filamentous, invisible in life; no cysts; in a pond in Lincolnshire, England. Bishop (1935) cultivated this flagellate in serum-saline medium, in hay infusion and in pond or rain water with boiled wheat grains at 4-31C. (Bishop,
1936, 1939).
flagella; a long adhering to body; nucleus anterior, without endosome; blepharoplast large, with a parabasal body and an axial

Genus Tricercomitus Kirby. Small; 3 anterior

flagellum,

trailing

filament; parasitic.
T. termopsidis K. (Fig. 167, b). 4-12/x by 2-3m; anterior flagella 6-20m long; trailing flagellum 19-65m long; in gut of Zootermopsis

POLYMASTIGINA
angusticollis, Z. nevadensis

391

and

Z. laticeps; California

and Arizona.

Culture and encystment (Trager, 1934). Genus Pentatrichomonas Mesnil. Similar to

Trichomonas, but

with 5 free anterior

flagella.

P. bengalensis Chatterjee. 9-20ju

by

7-14/*; in

human

intestine.

Kirby (1943, 1945a) observed that

of the five flagella, four arise

from

Fig. 167.
termopsidis,
d,

Trimastix convexa, X1310 (Hollande); c, Pentatrichomonoides scroa, Pseudotrypanosoma giganteum, X435 (Kirby).
a,

b,

Tricercomitus

X665 (Kirby)

X1500 (Kirby);

the end of a columnar (1-2ju long) extension, while the

is

fifth

flagellum

about 1m behind the extension. Genus Pentatrichomonoides Kirby. Five anterior flagella and the undulating membrane; axostyle very slightly developed; fusiform parabasal body; nucleus separated from the anterior blepharoplast;
a
little

shorter

and takes

its

origin

in termite gut.

P. scroa K. (Fig. 167, c). 14-45/u by 6-15/z; in Cryptotermes dudleyi and Lobitemies longicollis. Genus Pseudotrypanosoma Grassi. Large, elongate; 3 anterior flagella; undulating membrane; slender axostyle; band-like structure between nucleus and blepharoplast; parabasal body long, narrow;
in termite gut.

P. giganteum G. (Fig. 167, d). 55-lU/u long (Grassi); 145-205/*

by

392

PROTOZOOLOGY

20-40m; anterior flagella about 30m long (Kirby); in gut of Porotermes adamsoni and P. grandis.

Suborder 2 Diplomonadina

The suborder
sessing bilateral

consists of a

number

of binucleate flagellates pos-

symmetry.
Family Hexamitidae Kent

Genus Hexamita Dujardin (Octomitus Prowazek). Pyriform; 2 nuclei near anterior end; 6 anterior and 2 posterior flagella; 2 axo-

of

inflata, X600 (Klebs); b, c, trophozoite and cyst X1600 (Alexeieff); d, H. salmonis, X2100 (Davis); e, H. cryptocerci, X1600 (Cleveland); f, Trepomonas agilis, X1070 (Klebs); T. rotans, X710 (Lemmermann) h, Gyromonas ambulans, X530 g, (Seligo); i, Trigonomonas compressa, X490 (Klebs); j, Urophagus rostratus, X800 (Klebs).

Fig. 168.

a,

Hexamita

H.

intestinalis,

POLYMASTIGINA
styles; 1-2 contractile vacuoles in free-living forms;

393

scure;

endoplasm with

refractile granules;

cytostome obencystment; in stagnant

water or parasitic. H. inflata D. (Fig. 168, a). Broadly oval; posterior end truncate; 13-25/* by 9-1 5/z; in stagnant water. H. intestinalis D. (Fig. 168, b, c). 10-16/x long; in intestine of frogs, also in midgut of Trutta fario and in rectum of Motella tricirmustela in European waters. Morphology (Schmidt, rata and

1920).

H. salmonis (Moore)
pyloric caeca

(Fig. 168, d). 10-12/x

by

6-8/*; in intestine

of various species of trout

and salmon; schizogony

in epithelium of

and

intestine; cysts; pathogenic to

young host

fish

(Moore, 1922, 1923; Davis, 1925). H. periplanetae (Belaf). 5-8 m long; in intestine of cockroaches. H. cryptocerci Cleveland (Fig. 168, e). 8-13/t by 4-5. 5/z; in Cryptocercus punctulatus.

H. meleagridis McXiel, Hinshaw and Kofoid

6-12/x

(Fig. 169, a).

Body

by

2-5/*. It causes

a severe catarrhal enteritis in young tur-

keys. Experimentally

it is

transmitted to young quail, chicks, and

duckling (McNeil, Hinshaw and Kofoid, 1941).

H. sp. Hunninen and Wichterman (1938) (Fig. 169, b). Average dimensions 10/x by 5.5m; found in the reproductive organs of the
trematode, Deropristis
inflata, parasitic in

the eel; heavily infected

eggs are said not to develop.

soid; anterior

Genus Giardia Kunstler {Lamblia Blanchard). Pyriform to ellipend broadly rounded, posterior end drawn out; biconcave or

laterally symmetrical; dorsal side convex, ventral side

flat,

with a sucking disc in anterior half; 2 nuclei; 2 axostyles; 8 flagella in 4 pairs; cysts oval to ellipsoid; with 2 or 4 nuclei and
fibrils; in

the intestine of various vertebrates.

;

Many species.
;

Criteria

for species differentiation (Simon, 1921

Hegner, 1922) cytology and

taxonomy

(Filice, 1952).

G. intestinalis (Lambl) (G. enterica Grassi; G. lamblia Stiles (Fig.

169, c-g). When the flagella lash actively, the organism shows a slight forward movement with a sidewise rocking motion. The trophozoite is broadly pyriform, not plastic 9-20/x by 5-lG>; sucking disc acts as attachment organella; cytoplasm hyaline; 2 needle-like axostyles; 2 vesicular nuclei near anterior margin; 8 flagella in 4 pairs; two flagella originate near the anterior end of axostyles, cross each other and
;

follow the anterolateral margin of the disc, becoming free;

originating in anterior part of axostyles, leave the

two body about 1/3

from the posterior

tip;

two

(ventral)

originate in axostyles at nuclear level

which are thicker than others, and remain free; two (caudal)

394
flagella arise

PROTOZOOLOGY
from the posterior
tips of axostyles; a deeply staining

body may be found

in cytoplasm.

The

cysts are ovoid

fill

and

refractile; 8-14/x

by

6-lOju; cyst wall thin;

fibrils

contents do not

the wall; 2 or 4 nuclei, axostyles,

and

fla-

gella are visible in stained specimens.

This flagellate inhabits the lumen of the duodenum and other

of Deropristis inflata containing

Hexamita meleagridis, X1875 (McNeal et al.)\ b, an egg Hexamita, X770 (Hunninen and Wichterman); c-g, Giardia intestinalis, X2300 (c, front and d, side view of living organisms; e. stained trophozoite; f, fresh and g, stained mature
Fig. 169.
a,

cysts)

POLYMASTIGINA
parts of small intestine and colon of man.

395

Both trophozoites and

cysts are ordinarily found in diarrhoeic faeces. In severe cases of in-

an enormous number of the organisms attach themselves to mucous membrane of the intestine which may result in abnormal functions of the host tissues. In some cases, the flagellate has been reported from the gall bladder. The stools often contain unusual amount of mucus. Although there is no evidence that G. intestinalis
fection,

the

attacks the intestinal epithelium, experimental observations point to

its

pathogenicity (Tsuchiya and Andrews, 1930). Cytology (Kofoid

3-1 9m by 8-

and Swezy, 1922).

G. duodenalis (Davaine). In the intestine of rabbits;
1

U/x (Hegner, 1922). G. canis Hegner. In dogs; 12-17/x by 7.6-10/z; cysts oval, 9- 13m by

7-9m (Hegner, 1922). G. muris (Grassi). In rats and mice; 7-13m by 5- 10m (Simon, 1922). G. simoni Lavier. In the small intestine of rats; 14-19m by 7-10. 5m (Lavier, 1924); 1116/* by 5-8m (Nieschulz and Krijgsman, 1925). G. ondatrae Travis. In the intestine of the muskrat, Ondatra zibethica; 13m by 7m (Travis, 1939); 10m by 5.5m (Waters et al). G. caviae Hegner. In the intestine of guinea-pigs; 8-14m by 5.510m (Hegner, 1923).

Genus Trepomonas Dujardin. Free-swimming; flattened; more or rounded; cytostomal grooves on posterior half, one on each side; 8 flagella (one long and 3 short flagella on each side) arise from anterior margin of groove; near anterior margin there is a horseshoe-form structure, in which two nuclei are located; fresh water, parasitic,
less

or coprozoic.
T. agilis D. (Fig. 168, /). More or less ovoid; 7-30m long; 1 long and 3 short flagella on each side; rotation movement; stagnant water; also reported from intestine of amphibians. T. rotans Klebs (Fig. 168, g). Broadly oval; posterior half highly flattened; 2 long and 2 short flagella on each of 2 cytostomes; stag-

nant water.

'

Genus Gyromonas

Seligo.

Free-swimming; small; form constant,

flattened; slightly spirally coiled; 4 flagella at anterior end; cyto-

stome not observed; fresh water. G. ambulans S. (Fig. 168, h). Rounded; 8-15m long; standing
water.

cytostome on either
flagella; flagella

Genus Trigonomonas Klebs. Free-swimming; pyriform, side, from anterior margin of which
6 in
all;

plastic;

arise 3

2 nuclei situated near anterior end; move-

ment

rotation; holozoic; fresh water.

390
T. compressa

PROTOZOOLOGY
K.
(Fig. 168,
i).

24-33/x

by

10-16/*; flagella of differ-

ent lengths; standing water (King, 1936).

Genus Urophagus Klebs. Somewhat

nant water.
U. rostratus (Stein) (Fig. 168,
j).

similar to

Hexamita; but

a single cytostome; 2 moveable posterior processes; ho lo zoic; stag-

Spindle-form; 16-25/* by 6-12/*.

Suborder 3 Polymonadina

The polymonads are multinucleate. Each nucleus is associated with a blepharoplast (from which a flagellum extends), a parabasal

Fig. 170.

a,

Calonympha
senta,

grassii,
c,

X900

(Janicki); b,
clevelandi,
e,

Stephanonympha

nelumbium,
d,

X400 (Kirby);

Coronympha

Metacoronympha

X485 (Kirby);

X1000 (Kirby); Snyderella tabogae, X350

(Kirby).

POLYMASTIGINA
gont (Fig. 170, a)

397

body, and an axial filament. Janicki called this complex karyomastiand the complex which does not contain a nucleus, akaryomastigont (Fig. 170, e). This group includes the forms which inhabit the gut of various species of termites, most probably as
symbionts.

Genus Calonympha Foa. Body rounded; large; numerous long from anterior region; numerous nuclei; karyomastigonts and akaryomastigonts; axial filaments form a bundle; in termite
flagella arise

gut (Foa, 1905).

C. grassii F. (Fig. 170, a). 69-90/x long; in Cryptotermes grassii.

Genus Stephanonympha

Janicki.

Oval, but plastic; numerous

nuclei spirally arranged in the anterior half; karyomastigonts; axial

filaments form a bundle; in termite gut (Janicki, 1911).

S.

nelumbium Kirby

(Fig.

170, b). 45)u

by 27m;

in Cryptotermes

hermsi.

Genus Coronympha Kirby. Pyriform with 8 or 16

in a single circle in anterior region; 8 or 16

nuclei,

arranged

karyomastigonts; axoin

styles distributed; in termite gut (Kirby, 1929, 1939).

C. clevelandi
clevelandi.

K.

(Fig. 170, c).

25-53^ by 18-46/*;

Kalotermes

Genus Metacoronympha Kirby. Pyriform; one hundred or more karyomastigonts arranged in spiral rows meeting at the anterior end; each karyomastigont is composed of nucleus, blepharoplast, cresta, 3 anterior flagella, a trailing flagellum, and an axostyle; axostyle as in the last genus; in termite gut (Kirby, 1939). M. senta K. (Fig. 170, d). 22-92 M by 15-67ju; karyomastigonts about 66-345 (average 150) in usually 6 spiral rows; in Kalotermes
emersoni and four other species of the genus.

Genus Snyderella Kirby. Numerous nuclei scattered through the cytoplasm; akaryomastigonts close together and extend through the greater part of peripheral region; axial filaments in a bundle; in
termite gut (Kirby, 1929).
S. tabogae

K.

(Fig. 170, e).

conical anteriorly; 77-172ju

by

Pyriform; rounded posteriorly; bluntly 53-97/*; in Cryptotermes longicollis.

References

Alexeieff, A.: (1912) Sur quelques noms de genre des

Zool. Anz., 39:674.

flagelles,

etc

Andai, G.: (1933) Ueber Costia necatrix. Arch. Protist., 79:284. Andrews, J. and Miller, F. W.: (1936) Non-venereal transmission of Trichomonas foetus infection in cattle. Am. J. Hyg., 24:433. - (1938) Trichomonas foetus in bulls. Ibid., 28:40.

398

PROTOZOOLOGY
and Rees, C. W.
:

(1936) Experimental Trichomonas foetus infection in sheep. J. Parasit., 22:108. Andrews, Mary N.: (1929) Observations on Trichomonas vaginalis,

Barnes, W.

Trop. Med. Hyg., 32:237. B.: (1951) Trichomoniasis in mourning doves in Indiana. Indiana Audub. Quart., 29:8. Bartlett, D. E.: (1947) Trichomonas foetus infection and bovine reproduction. Am. J. Vet. Res., 8:343. (1948) Bovine venereal trichomoniasis: etc. Proc. U. S. Livestock Sanit., A. 1947, p. 170. Becker, E. R. (1933) Two observations on helminths. Tr. Am. Micr. Soc, 52:361. Belar, K: (1921) Protozoenstudien. III. Arch. Protist., 43:431. Bishop, Ann: (1930) The action of HC1 upon cultures of Trichomonas. Parasitology, 22:230. (1931) The morphology and method of division of Trichomonas. Ibid., 23:129. (1934) The experimental infection of Amphibia with cultures of Trichomonas. Ibid., 26:26. (1935) Observations upon a "trichomonas" from pond water. Ibid., 27:246. (1936) Further observations upon a "Trichomonas" from pond water. Ibid., 28:443. (1939) A note upon the systematic position of "Trichomonas" keilini. Ibid., 31:469. Boeck, W. C: (1921) Chilomastix mesnili and a method for its culture. J. Exper. Med., 33:147. and Tanabe, M.: (1926) Chilomastix gallinarum, morphology, division and cultivation. Am. J. Hyg., 6:319. Bunting, Martha: (1926) Studies of the life-cycle of Tetramitus rostratus. J. Morphol. Physiol., 42:23. and Wenrich, D. H.: (1929) Binary fission in the amoeboid and flagellate phases of Tetramitus rostratus. Ibid., 47:37. Cleveland, L. R.: (1935) The intranuclear achromatic figure of Oxymonas grandis sp. nov. Biol. Bull., 69:54. (1938) Mitosis in Pyrsonympha. Arch. Protist,, 91:452.
etc. J.
:

(1950) Hormone-induced sexual cycle of flagellates.

II. J.

Morphol., 86:185.
(1950a) III. Ibid., 86:215. (1950b) IV. Ibid., 87:317. Hall, S. R., Sanders, E. P. and Collier, J.: (1934) The wood-feeding roach, Cryptocercus, its Protozoa, etc. Mem. Am. Acad. Arts and Sc, 17:185. Connell, F. H.: (1930) The morphology and life-cycle of Oxymonas dimorpha, etc. Univ. daiifornia Publ. Zool., 36:51. da Fonseca, O. O. R.: (1915) Sobre os flagellados dos mammiferos do Brazil. Brazil Medico, 29:281. Davis, H. S.: (1925) Octomitus salmonis, a parasitic flagellate of trout. Bull. Bur. Fisher., 42:9. (1943) A new polymastigine flagellate, Costia pyriformis, parasitic on trout. J. Parasit., 29:385.

POLYMASTIGINA
Dobell, C: (1934) Researches on the intestinal Protozoa keys and man. VI. Parasitology, 26:531.
of

399

mon-

(1935) VII. Ibid., 27:564. (1939) The common flagellate of the human mouth, Trichomonas tenax (O.F.M.): etc. Ibid., 31:138. -and O'Connor, F. W.: (1921) The intestinal Protozoa of

man. London. Dogiel, V.: (1916) Researches on the parasitic Protozoa from the
intestine of termites. I. J. russ. zool., 1:1. A.: (1836) Animalcules observes dans les matieres purulentes et le produit des secretions des organes genitaux de l'homme et de la femme. C. R. Acad. Sc, 3:385. Duboscq, O. and Grasse, P.: (1925) Appareil de Golgi, mitochondries, etc. C. R. Soc. Biol., 93:345. Feo, L. G. (1944) The incidence and significance of Trichomonas vaginalis in the male. Am. J. Trop. Med., 24:195. Filice, F. P.: (1952) Studies on the cytology and life history of a Giardia from the laboratory rat. Uni. Cal. Publ. Zool., 57:53. FoA, Anna: (1905) Due nuovi flagellati parassiti (Nota prelim.).

Donne,

Rend. Ace. Lincei, 14:542. Galli-Valerio, B. (1903) Notes de parasitologic. Centralbl. Bakt.
:

I.

Orig., 35:81.

Geiman, Q. M.: (1935) Cytological studies of the Chilomastix of man and other mammals. J. Morphol., 57:429. Grasse, P. P.: (1926) Contribution a l'etude des flagell^s parasites.

de Trichomonadines. Grasse Ordre and Faure, Alice: Quelques donnees

1.

Arch. zool. exper. gen., 65:345. zoologie. I. Fasc. (1952) Traite des (1952a)

Paris.

In:

(1952), p.

704.

la cytologie et la

nouvelles sur (1939) reproduction de Trichomonas caviae. Bull. biol.

France et Belg., 73: 1. Grassi, B.: (1917) Flagellati nei Termitidi.

Mem.

R. Ace. Lincei,

(1911) Intorno ai protozoi dei termitidi S. V. CI. Sc. fils, 20:725. Hawes, R. S.: (1947) On the structure, division, and systematic position of Trichomonas vaginalis Donne, with a note on its methods of feeding. Quart. J. Micr. Sc, 88:79. comparative study of the Giardias living Hegner, R. W. (1922) in man, rabbit, and dog. Am. J. Hyg., 2:442. (1923) Giardias from wild rats and mice and Giardia caviae sp. n. from the guinea-pig. Ibid., 3:345. Hogue, Mary J.: (1938) The effect of Trichomonas foetus on tissue culture cells. Am. J. Hyg., 28:288. (1943) The effect of Trichomonas vaginalis on tissue culture
(n.p.).

-and FoA,
:

Ser. 5, 12:331.

Anna:

Rend. R. Ace. Lincei,

cells. Ibid.,

37:142.

Hollande, A.
Hsiung, T.

V.: (1939) Sur

un genre nouveau de Trichomonadide

France, 64:114. on the Protozoa of the large intestine of the horse. Iowa State College J. Sc, 4:356.
libre: etc. Bull. soc. zool. S.: (1930)

A monograph

400

PROTOZOOLOGY
:

Hunninen, A. V. and Wichterman, R. (1938) Hyperparasitism: a species of Hexamita found in the reproductive systems, etc.
Janicki,
24:95. (1911) Zur Kenntnis des Parabasalapparats bei parasitischen Flagellaten. Biol. Centralbl., 31:321. (1915) Untersuchungen an parasitischen Flagellaten. II. Ztschr. wiss. Zool., 112:573. Kimura, G. G.: (1934) Cochlosoma rostratum sp. nov., etc. T. Am.
J. Parasit.,

C:

Micr. Soc, 53:102. Kirby, H. Jr.: (1924) Morphology and mitosis

of

Dinenympha

Jimbriata. Univ. California Publ. Zool., 26:199. (1926) On Staurojoenina assimilis sp.n. Ibid., 29:25. (1926a) The intestinal flagellates of the termite, Cryptotermes hermsi. Ibid., 29:103. (1928) species of Proboscidiella from Kalotermes, etc.

Quart. J. Micr. Sc, 72:355. (1929) Snyderella and Coronympha, etc. Uni. Cal. Publ. Zool., 31:417. (1930) Trichomonad flagellates from termites. I. Ibid., 33:

393

(1931) II. Ibid., 36:171. (1932) Two Protozoa from brine. Tr. Am. Micr. Soc, 51:8. (1936) Two polymastigote flagellates of the genera Pseudo-

devescovina and Caduceia. Quart. J. Micr. Sc, 79:309. (1937) The devescovinid flagellate Parajoenia grassii from a Hawaiian termite. Univ. California Publ. Zool., 41:213. (1938) Polymastigote flagellates of the genus Foaia Janicki, etc. Quart. J. Micr. Sc, 81:1. (1939) Two new flagellates from termites in the genera Coronympha Kirby, etc. Proc California Acad. Sc, 22:207. (1941) Devescovinid flagellates of termites. I. Univ. Cali-

(1942a) III. Ibid., 45:167. (1943) Observations on a trichomonad from the intestine of J. Parasit., 29:422. (1944) Some observations on cytology and morphogenesis in flagellate Protozoa. J. Morphol, 75:361. (1945) The structure of the common intestinal trichomonad of man. Jour. Parasit., 31:163. (1946) Gigantomonas herculea. Uni. Cal. Publ. Zool., 53:163. (1947) Flagellate and host relationships of trichomonad flagellates. J. Parasit., 33:214. (1949) Devescovinid flagellates of termites. V. Univ. California Publ. Zool., 45:319. (1951) Observations on the trichomonad flagellate of the reproductive organs of cattle. J. Parasit., 37:445. and Honigberg, B.: (1949) Flagellates of the caecum of ground squirrels. Univ. California Publ. Zool., 53:315. Klug, G.: (1936) Neue oder wenig bekannte Arten der Gattungen Mastigamoeba, etc Arch Protist., 87:97.

man.

fornia Publ. Zool., 45:1. (1942) II. Ibid., 45:93.

POLYMASTIGINA
tiple fission in

401

Kofoid, C. A. and Christiansen, E. B.: (1915) On binary and mulGiardia muris. Univ. California Publ. Zool., 16:
30.

- and Swezy, Olive: (1915) Mitosis and multiple fission in trichomonad flagellates. Proc. Am. Acad. Arts and Sc,
51:289.
(1920)

On

the morphology and mitosis of Chilomastix

mesnili, etc. Univ. California Publ. Zool., 20:117. (1922) Mitosis and fission in the active and encysted phases of Giardia enterica, etc. Ibid., 20:199. - (1920) On Proboscidiclla multinucleata, etc. Ibid., 20:

301.

Koidzumi, M.: (1921) Studies on the intestinal Protozoa found

in

the termites of Japan. Parasitology, 13:235. Kotlan, A.: (1923) Zur Kenntnis der Darmflagellaten aus der Hausente und anderen Wasservogeln. Centralbl. Bakt. I. Orig., 90:24. Kozloff, E. N.: (1945) The morphology of Trichomonas limacis. J. Morphol., 77:53. Kuczynski, M. H.: (1918) Ueber die Teilungsvorgange verschiedener Trichomonaden, etc. Arch. Protist., 39:107. Lambl, W. (1859) Mikroskopische Untersuchungen der DarmExcrete. Vierteljahrschr. prakt. Heilk., 61:1. Lavier, G.: (1924) Deux especes de Giardia, etc. Ann. Parasit., 2:
:

161.

Leidy, J.: (1877) On intestinal parasites of Tcrmes flavipes. Proc. Acad. Nat. Sc, Philadelphia, p. 146. Levine, N. D., Boley, L. E. and Hester, H. R.: (1941) Experimental transmission of Trichomonas gallinae from the chicken to other birds. Am. J. Hyg., 33:23. and Brandly, C. A.: (1940) Further studies on the pathogenicity of Trichomonas gallinae for baby chicks. Poultry Sc,

19:205.
S. F.: (1926) On Metadevescovina debilis g. n., sp. n. Univ. California Publ. Zool., 29:141. Lynch, K. M.: (1922) Tricercomonas intestinalis and Enter omonas caviae n. sp., etc. J. Parasit., 9:29. Martin, C. H. and Robertson, Muriel: (1911) Further observations on the caecal parasites of fowls. Quart. J. Micr. Sc, 57:53. McNeil, Ethel and Hinshaw, W. R.: (1942) Cochlosoma rostratum from the turkey. J. Parasit., 28:349. and Kofoid, C. A.: (1941) Hexamita meleagridis sp. nov. from the turkey. Am. J. Hyg., 34:71. Moore, Emmeline: (1922) Octomitus salmonis, a new species of intestinal parasite in trout. Tr. Am. Fish. Soc, 52:74. (1923) Diseases of fish in State hatcheries. Rep. Bur. Prev. Stream Poll., New York, 12:18. Morgan, B. B. and Noland, L. E.: (1943) Laboratory methods for differentiating Trichomonas foetus from other Protozoa in the diagnosis of trichomoniasis in cattle. J. Am. Vet. Med. Assoc, 102:11.

Light,

402

PROTOZOOLOGY

Nie, D.: (1950) Morphology and taxonomy of the intestinal Protozoa of the guinea-pig, Cavia porcella. J. Morphol., 86:381. Nieschulz, O. and Krijgsman, B. J.: (1925) Ueber Giardia simoni Lavier. Arch. Protist., 52:16(5. Powell, W. N.: (1928) On the morphology of Pyrsonympha with a description of three new species, etc. Univ. California Publ. Zool., 31:179. Rees, C. W. (1938) Observations on bovine venereal trichomoniasis. Veter. Med., 33:321. Reuling, F.: (1921) Zur Morphologie von Trichomonas vaginalis. Arch. Protist., 42:347.
:

On the viability of Tritrichomonas augusta. Micr. Soc, 55:313. Samuels, R. (1941) The morphology and division of Trichomonas augusta. Ibid., 60:421. Schmidt, W.: (1920) Untersuchungen iiber Octomitus intestinalis. Arch. Protist., 40:253. Simon, C. E.: (1921) Giardia enterica: etc. Am. J. Hyg., 1:440. (1922) A critique of the supposed rodent origin of human giardiasis. Ibid., 2:406. Stabler, R. M.: (1941) The morphology of Trichomonas gallinae ( = columbae). J. Morphol, 69:501. (1951) Effect of Trichomonas gallinae from diseased mourning doves on clean domestic pigeons. J. Parasit., 37:473. and Engley, F. B.: (1946) Studies on Trichomonas gallinae infections in pigeon squabs. J. Parasit., 32:225. Feo, L. G. and Rakoff, A. E.: (1941) Implantation of intestinal trichomonads (T. hominis) into the human vagina. Am. J. Hyg., 34:114. and Pennypacker, M. I.: (1939) A brief account of Trichomonas augusta, etc. Tr. Am. Micr. Soc, 58:391. Sutherland, J. L.: (1933) Protozoa from Australian termites. Quart, J. Micr. Sc, 76:145. Tavolga, W. N. and Nigrelli, R. F.: (1947) Studies on Costia necatrix. Tr. Am. Micr. Soc, 66:366. Theiler, H. and Farber, S. M.: (1932) Trichomonas muris, parasitic in Oxyurids of the white mouse. J. Parasit., 19: 169. Trager, W. (1934) A note on the cultivation of Tricercomitus termopsidis, etc. Arch. Protist., 83:264. Travis, B. V. (1932) A discussion of synonymy in the nomenclature of certain insect flagellates, etc. Iowa State College J. Sc, 6:317. (1932a) Trichomonas phasiani, a new flagellate from the ring-necked pheasant, etc. J. Parasit., 18:285. (1934) Karotomorpha, a new name for Tetramastix, etc. Tr. Am. Micr. Soc, 53:277. (1939) Descriptions of five new species of flagellate Protozoa of the genus Giardia. J. Parasit., 25:11. Trussell, R. E.: (1947) Trichomonas vaginalis and trichomoniasis.
Rosenberg,
Tr.
L. E.: (1936)

Am.

Springfield, Illinois.

and Johnson,

G.: (1945) Trichomonas vaginalis Donne. Re-

POLYMASTIGINA

403

cent experimental advances. Puerto Rico J. P. H. Trop. Med., 20:289. Tsuchiya, H. and Andrews, J. (1930) A report on a case of giardiasis. Am. J. Hyg., 12:297. Waters, P. C. Fiene, A. R. and Becker, E. R.: (1940) Strains in Giardia ondatrae Travis. Tr. Am. Micr. Soc, 59:160. Weissenberg, R. (1912) Callimastix cyclopis n.g., n.sp., etc. Berlin. Sitz.-Ber. Ges. naturf. Freunde, p. 299. Wenrich, D. H.: (1921) The structure and division of Trichomonas muris. J. Morphol., 36:119. (1932) The relation of the protozoan flagellate, Retortamonas gryllotalpae, etc. Tr. Am. Micr. Soc, 51:225. (1944) Comparative morphology of the trichomonad flagellates of man. Am. J. Trop. Med., 24:39. (1944a) Morphology of the intestinal trichomonad flagellates
: :

in
J.

man and
(1947)

of similar

forms in monkeys,

cats,

dogs and
J.

rats.

Morphol., 74:189.

The

species of

Trichomonas

in

man.

Parasit.,

33:177.

and Emmerson, M. A.: (1933) Studies on the morphology of Tritrichomonas foetus (Riedmiiller) from American cows. J. Morphol., 55:193. -and Saxe, L. H.: (1950) Trichomonas microti n.sp. J. Parasit., 36:261. Wenyon, C. M.: (1926) Protozoology. 1. London and Baltimore. Zeliff, C. C: (1930) A cytological study of Oxymonas, etc. Am. J. Hyg., 11:714. (1930a) KirbyeUa zeteki, etc. Ibid., 11:740.

Chapter

16

Order 4 Hypermastigina Grassi and Foa

ALL
.

members

of this order are inhabitants of the alimentary

canal of termites, cockroaches, and woodroaches. The cytoplasmic organization is of high complexity, although there is only a single nucleus. Flagella are numerous and have their origin in the

blepharoplasts located in the anterior region of body. In

cies

many

spe-

which are xylophagous, there exists a true symbiotic relationship between the host termite and the protozoans (p. 29). Method of nutrition is either holozoic or saprozoic (parasitic). Bits of wood, starch grains, and other food material are taken in by means of pseudopodia (p. 99). Asexual reproduction is by binary fission; multiple division has also been noted in some species under certain conditions, while sexual reproduction has been observed in a few species. Encystment occurs in some genera of Lophomonadidae and certain species inhabiting woodroaches in which moulting of the host insect leads to encystment and sexual reproduction. The protozoan fauna of the colon is lost at the time of molting of the host insect, but newly molted individuals regain the fauna by proctodeal feeding (Andrews, 1930). The number of Protozoa present in the colon of the termite is usually very enormous. The total weight of all Protozoa present in a termite worker has been estimated to be from about 1/7-1/4 (Hungate, 1939) or 1/3 (Katzin and Kirby, 1939) to as much as 1/2
(Cleveland, 1925) of the

body weight

of the host.

The

correlation-

ship between the termite and

its intestinal flagellate

fauna, has been

studied by several observers. Kirby (1937) notes that certain groups of flagellates occur only in certain groups of termites, while others are widely distributed. Flagellates of one host termite introduced
into individuals of another species survive for a limited time only

(Light and Sanford, 1928; Cleveland, Hall

1941, 1940).
1928).

et al.,

1934; Dropkin,

Taxonomy (Koidzumi,

1921; Kirby, 1920; Bernstein,

Body without segmented appearance

Flagella in spiral rows Family Flagella not arranged in spiral rows Flagella in one or more anterior tufts
1 tuft of flagella 2 tufts of flagella 4 tufts of flagella
1

Holomastigotidae

(p.

405)

Several tufts (loriculae)

Family 2 Lophomonadidae Family 3 Hoplonymphidae Family 4 Staurojoeninidae Family 5 Kofoidiidae

404

(p.
(p.

(p. (p.

407) 410) 412) 412)

HYPERMASTIGINA
Flagella not arranged in tufts Posterior part without flagella

405

Family 6 Trichonymphidae
Flagella over entire body.. .Family 7

(p. (p. (p.

Eucomonymphidae
8 Teratonymphidae

Body with segmented appearance. .Family

Family
1

412) 414) 414)

Holomastigotidae Janicki

Genus Holomastigotes Grassi. Body small; spindle-shaped; few spiral rows reach from anterior to posterior end; nucleus anterior, surrounded by a mass of dense cytoplasm; saprozoic; in the termite
gut.

H. elongatum G.
70/x

(Fig. 171, a).

In gut of Reticulitermes lucifugus,

R. speratus, R. flaviceps, and Macrohodotermes massambicus; up to

by 24m

(Grassi, 1892).

X700 (Koidzumi); b, HoloX250 (Koidzumi); c, Spirotrichonympha leidyi, X400 (Koidzumi); d, S. pulchella, X900 (Brown); e, Microspirotrichonympha porteri, X250 (Koidzumi); f, M. ovalis, X600 (Brown); g, Macrospironympha xylopletha, X300 (Cleveland et al.); h, Leptospironympha eupora, X1050 (Cleveland et al.).
Fig.
171. a,

Holomastigotes elongatum,

mastigotoides hartmanni,

406

PROTOZOOLOGY

Genus Holomastigotoides Grassi and Foa. Large; pyriform; spiral rows of flagella as in the last genus, but more numerous (12-40 rows) a mass of dense cytoplasm surrounds ovoid nucleus near the anterior end; in termite gut (Grassi and Foa, 1911). Cytology (Cleve;

land, 1949).

H. hartmanni Koidzumi
termes formosanus.

(Fig.

171, b).

50-140^ long;
a, 6).

in Copto-

H.
form;

tusitala

Cleveland (Figs. 62; 63; 64; 172,

In the hindgut

of Prorhinotermes simplex; largest species in this host; elongate pyrifive flagellar bands, arise at the anterior end and spiral the body 5| times; dimorphic with respect to chromosome numbers, 2 and 3; 130-200 m long. Cleveland's observation on its chromosome

cycle has been mentioned elsewhere (p. 158).

Genus Spirotrichonympha Grassi and Foa (1911). Moderately embedded in cytoplasm in anterior region, arising from 1 to several spiral bands; mass of dense cytoplasm conical and its base indistinct; nucleus spherical; in termite gut. Development (Duboscq and Grasse, 1928). S. leidyi Koidzumi (Fig. 171 ,c). In Coptotermes formosanus; 15-50/z by 8-30ju. S. pulchella Brown (Fig. 171, d). 36-42 M by 14-16/x; in Reticularge; elongate pyriform; flagella deeply

litermes hageni.
S. bispira Cleveland. In

32-48m; two

flagellar

bands

in

Kalotermes simplicicornis ; 59-102^ by 34 spiral turns; resting nucleus with

two chromosomes; the cytoplasmic division is unique in that portion of the anterior end shifts its position to the posterior end, where a new flagellar band develops; thus the division is longitudinal (Cleveland, 1938).

Genus Spirotrichonymphella
flagella long; saprozoic,

Grassi. Small; without spiral ridges;

not wood-feeding; in termite gut.

S.

pudibunda G. In Porotermes adamsoni; Australia. Multiple

fusion (Sutherland).

Genus Micro spirotrichonympha Koidzumi (Spironympha Koidzumi). Small, surface not ridged; spiral rows of flagella only on anterior half; a tubular structure between nucleus and anterior

extremity; a mass of dense cytoplasm surrounds nucleus; with or without axial rod; in termite gut (Koidzumi, 1917, 1921).

M.

porteri

K. (Fig. 171,

e).

In Reticulitermes flaviceps ; 20-55^ by

20-40m.

M.

litermes hesperus

(Brown) (Fig. 171,/). 36-48/1 by about 40/z; in Reticu(Brown, 1931). Genus Spirotrichosoma Sutherland. Pyriform or elongate; below
ovalis

HYPERMASTIGINA

407

operculum, two deeply staining rods from which fiagella arise and which extend posteriorly into 2 spiral flagellar bands; without axostyle; nucleus anterior, median; wood chips always present, but

method

of feeding

S. capitata S. 87/x

unknown; by 38/*;

in Stolotermes victoriensis; Australia.

flagellar

bands closely

spiral,

reach

posterior end.
et al. Broadly conical: fiaon 2 broad flagellar bands which make 10-12 spiral turns, 2 inner bands; axostyles 36-50 or more; during mitosis nucleus migrates posteriorly; encystment, in which only nucleus and centrioles are retained, takes place at each ecdysis of host; in Cryptocercus punctu-

Genus Macrospironympha Cleveland

gella

latus.

M.
gella

xylopletha C.

et al.

(Fig. 171, g).

112-154 M by 72-127 M
et al.

Genus Leptospironympha Cleveland

Cylindrical; small; fiaaxis; axostyle single,

on 2 bands winding spirally along body

hyaline; in Cryptocercus punctulatus. Several species. Sexual repro-

duction (Cleveland, 1951). L. eupora C. et al. (Fig. 171,

h). 30-38/z by 18-21/i. Genus Rostronympha Duboscq, Grasse and Rose. Form

variable,

ovoid to medusoid; with or without a long contractile attaching organelle like a trunk, constricted in three places and of annulated
surface; spiral ridges

from which

fiagella arise,

terior half; posterior half with attached spirochaetes;

in

do not reach the posxylophagous;

the intestine of Anacanthotermes in Algier.

magna D., G. and R. (Fig. 172, c-e). Large individuals, 135180m by 110-135/x, with the trunk-like extension reaching a length of 180yu; the body proper is divided into two parts; the posterior portion may be drawn out like the manubrium of a medusa; axostyle conspicuous; in the gut of Anacanthotermes ochraceus of Algier (Duboscq
R.

and Grasse, 1943). Family 2 Lophomonadidae Kent

Genus Lophomonas mon;

Stein.

nucleus anterior; axostyle composed of

in colon of cockroaches.

Ovoid or elongate; small: a vesicular many filaments; cysts com-

L. blattarum S. (Figs. 24, a; 65; 72; 173, a-e). Small pyriform,

plastic;

bundle of axostylar filaments may project beyond the posmovements; binary or multiple fission; 25-30/1 long; encystment; holozoic; in the colon of cockroaches, Blatta orientalis in particular; widely distributed (Kudo, 1926). Cytology (Jaterior end; active
nicki, 1910; Belaf, 1926;

Kudo,

1926).

L. striata Biitschli (Fig. 173, f-h). Elongate spindle;

body with

408

PROTOZOOLOGY
some
investigators

obliquely arranged needle-like structures which

believe to be a protophytan (to which Grasse gave the name, Fusi-

formis lophomonadis) ; bundle of axial filaments short, never protruding; movement sluggish; cyst spherical with needle-like structures;
in

same habitat as the

last species.

Cytology (Kudo, 1926a).

&-

'

Holomastigotoides tusitala (Cleveland) (a, surface view; parabasal bodies, thin axostyles) c-e, Rostronympha magna (Duboscq and Grasse) (c, a large individual with the completely extended trunk, with axostyle, X500; d, a small medusoid form, XI 000; e, a young individual with posteriorly attached spirochaetes, X500); f, anterior end of Joenia annectens (Duboscq and Grasse).
Fig. 172.
a, b,

b,

flagellar bands,

flagella

Genus Eulophomonas Grassi and Foa. Similar to Lophomonas, but vary from 5-15 or a little more in number; in termite gut.

E. kalotermitis Grassi. In Kalotermes flavicollis; this flagellate has not been observed by other workers. Genus Prolophomonas Cleveland et al. Similar to Eulophomonas; established since Eulophomonas had not been seen by recent observers; it would become a synonym "if Eulophomonas can be found in

K.

flavicollis"

(Cleveland

et al.).

HYPERMASTIGINA
P. tocopola C.
et al.

409

(Fig. 173,

i).

14-19/i

by

12-15/*; in Cr?/pto-

cercus punctidatus.

Genus Joenia Grassi. Ellipsoidal; anterior portion capable of forming pseudopodia; flagellar tufts in part directed posteriorly; surface covered by numerous immobile short filamentous processes,

Fig. 173. a-e, Lophomonas blattarum (a, b, in life, X320; c, a stained d, a trophozoite in which the nucleus is dividing; e, a stained cyst, X1150) (Kudo); f-h, L. striata (f, in life, X320; g, a stained dividing individual; h, a stained cyst, XI 150) (Kudo); i, Prolophomonas tocopola, X1200 (Cleveland et al.); j, Joenia annectens (Grassi and Foa); k, Microjoenia pyriformis, X920 (Brown); 1, Torquenympha octophis, X920

specimen;

(Brown).

nucleus spherical, anterior; posterior to

it

a conspicuous axostyle

composed
rounding

of
it;

numerous

axial filaments, a parabasal apparatus sur-

J. annectens G. (Figs. 172, /; 173, j). In

xylophagous; in termite gut (Grassi, 1885). Kalotermes

flavicollis.

Parabasal apparatus (Duboscq and Grasse, 1928a).

410

PROTOZOOLOGY

Genus Joenina Grassi. More complex in structure than that of Joenia; flagella inserted at anterior end in a semi-circle; parabasal
bodies 2 elongated curved rods; xylophagous (Grassi, 1917).
J. pulchella G. In Porotermes adamsoni.

Genus Joenopsis

Cutler. Oval; large; a horseshoe-shaped pillar at

it;

anterior end, flagella arising from

some directed

anteriorly, others

posteriorly; parabasal bodies long rods; a strong axostyle; xylopha-

gous; in the termite gut (Cutler, 1920).

J. polytricha C. In Archotermopsis wroughtoni; 95-129/z long.

Genus Microjoenia
body simple;

Grassi.

Small, pyriform; anterior end

flat-

tened; flagella arranged in longitudinal rows; axostyle; parabasal

in termite gut (Grassi, 1892).

M.

pyriformis

Brown

(Fig. 173, k).

44-52 n by 24-30/x;

in Reticuli-

termes hageni (Brown, 1930).

Genus Mesojoenia Grassi and Foa. Large; flagellar tuft spreads over a wide area; distinct axostyle, bent at posterior end; 2 parabasal bodies; in termite gut (Grassi and Foa, 1911).

decipiens G. In Kalotcrmes flavicollis.

Genus Torquenympha Brown. Small; pyriform or top-form; axostyle; radially

symmetrical; 8 radially arranged parabasal bodies;

nucleus anterior; in termite gut (Brown, 1930). T. octoplus B. (Fig. 173, I). 15-26/x by 9-13/z; in Reticulitermes

Family 3 Hoplonymphidae Light

Genus Hoplonympha Light. Slender fusiform, covered with thick, rigid pellicular armor; each of the two flagellar tufts arises from a
plate connected with blepharoplast at anterior end; nucleus near

anterior extremity,
(Light, 1926).

more or

less triangular in

form; in termite gut

5-12/x; in Kalotermes

H. natator L.
simplicicornis.

(Fig. 174, a, b). 60-120/x

by

Genus Barbulanympha Cleveland

et al.

row, nuclear sleeve between centrioles;

number

Acorn-shaped: small, narof rows of flagella

greater at base; large chromatin granules;

numerous (80-350) para-

basals; axostylar filaments 80-350; flagella 1500-13,000; different

species

of chromosomes during mitosis; in gut Four species. B. ujalula C. et al. (Figs. 61; 174, c). 250-340 M by 175-275 M 50 chromosomes; flagellated area 36-41ju long; centriole 28-35^ long. B. laurabuda C. et al. 180-240^ by 135-170/z; 40 chromosomes; flagellated area 29-33/z long; centriole 24-28^ long.

show

different

number

of Cryptocercus punctulatus.

HYPERMASTIGINA
gellar

411

Genus Rhynchonympha Cleveland et al. Elongate; number of flarows same throughout; axial filaments somewhat larger and
2400
flagellar in Cryplocercus

longer, about 30; 30 parabasals:

tulatus.

punc-

Sexual cycle (Cleveland, 1952). R. tarda C. et al. (Fig. 175,/). 130-215 M by 30-70 M Genus Urinympha Cleveland et at. Narrow, slender; flagellated area, smaller than that of the two genera mentioned above; flagella move as a unit; about 24 axial filaments; 24 parabasals; 600 flagella;
.

Hoplonympha natator, X450 (Light); c, Barbulanympha X210 (Cleveland etal.); d, Urinympha talea, X350 (Cleveland et al.); e, Staurojoenina assimilis, X200 (Kirby); f, Idionympha perissa, X250 (Cleveland et al.); g, Teratonympha mirabilis, X200 (Dogiel).
Fig. 174. a, b,
ufalula,

412

PROTOZOOLOGY

in gut of Cryptocercus punctulatus (Cleveland, 1951a).

U. talea C. (Fig. 174, d). 7 5-300 /i by 15-50/t; sexual reproduction (Cleveland, 1951a).

Family 4 Staurojoeninidae Grassi

Genus Staurojoenina
rior

Grassi. Pyriform to cylindrical;

anterior

region conical; nucleus spherical, central; 4 flagellar tufts from ante-

end; ingest

wood fragments;
(Fig.

in termite gut (Grassi, 1917).

S. assimilis

Kirby

174, e).

105-190/z long; in Kalotermes

minor (Kirby, 1926). Genus Idionympha Cleveland et al. Acorn-shaped; axostyles 8-18; fine parabasals grouped in 4 areas; pellicle non-striated; nucleus nearer anterior end than that of Staurojoenina; flagellated areas smaller; in gut of Cryptocercus punctulatus.
I. perissa C.
et.

al (Fig. 174,/). 169-275/*

by

98-155/t.

Family 5 Kofoidiidae Light

Genus Kofoidia Light. Spherical;

loriculae

flagellar tufts

composed

of 8-16

(permanently fused bundles of flagella); without either axostyle or parabasal body; between oval nucleus and bases of flagellar tufts, there occurs a chromatin collar; in termite gut (Light,
1927).

K.

loriculata L. (Fig. 175, a, b). 60-140/z in diameter; in Kalotermes

simplicicornis.

Family 6 Trichonymphidae Kent

Genus Trichonympha Leidy (Leidyonella Frenzel; Gymnonympha Dobell; ? Leidy opsis Kofoid and Swezy). Anterior portion consists of nipple and bell, both of which are composed of 2 layers; a distinct
axial core; nucleus central; flagella located in longitudinal
bell;

rows on

xylophagous; in the intestine of termites and woodroach. Many species. The species inhabiting the woodroach undergo sexual reproduction at the time of molting of the host (Cleveland, 1949a)
185). Species (Leidy, 1877; Kirby, 1932, 1944)
;

(p.

nomenclature (Cleveland, 1938; Dobell, 1939); mineral ash (MacLennan and Murer,
1934).
T.

campanula Kofoid and Swezy

(Figs. 60; 175, c). 144-313/z

57-1 44/t;
(Fig.

wood
a);

particles are taken in

by

posterior region of the

35,

in Zootermopsis

angusticollis,

by body Z. nevadensis and Z.

(Kofoid and Swezy, 1919). T. agilis Leidy (Fig. 175, d). 55-1 15/t by 22-45/*; in Reticulitermes flavipes, R. lucifugus, R. speratus, R. flaviceps, R. hesperus, R. tibialis.
laticeps

(Leidy, 1877).

HYPERMASTIGINA
T. grandis Cleveland
et al.

413
in Cryptocercus

190-205^ by 79-88^;

punctulatus.

Genus Pseudotrichonympha Grassi and Foa. 2 parts in anterior end as in Trichonympha; head organ with a spherical body at its tip and surrounded by a single layer of ectoplasm; bell covered by 2
layers of ectoplasm; nucleus lies freely;

body covered by

slightly

Fig. 175. a, b, Kofoidia loriculata, X175, X300 (Light); c, Trichonympha campanula, X150 (Kofoid and Swezy); d, T. agilis, X410 (Kirby); e, Eucomonympha imla, X350 (Cleveland et al.); f, Rhynchonympha tarda, X350 (Cleveland et al.).

414

PROTOZOOLOGY

oblique rows of short fiagella; in termite gut (Grassi and Foa, 1911). P. grassii Koidzumi. In Coptotermes formosanus; spindle-form;

200-300^ by 50-1 20/x (Koidzumi, 1921). Genus Deltotrichonympha Sutherland. Triangular; with a small dome-shaped "head"; composed of 2 layers; head and neck with long active fiagella; body fiagella short, arranged in 5 longitudinal rows; fiagella absent along posterior margin; nucleus large oval, located in anterior third; cytoplasm with wood chips; in termite gut. One
species.

in

D. operculata S. Up to 230/* long, 164/* wide, and about gut of Mastotermes darwiniensis; Australia.

50/x thick;

Family 7 Eucomonymphidae Cleveland

et al.

Genus Eucomonympha Cleveland

et al.

Body covered with

fiagella

arranged in 2 (longer rostral and shorter post-rostral) zones; rostral tube very broad, filled with hyaline material; nucleus at base of
rostrum; in gut of Cryptocercus punctulatus.
E. imla C. et al. (Fig. 175, e). 100-165/* by 48-160/*; attached forms more elongate than free individuals; sexual reproduction
(Cleveland, 1950).

Family 8 Teratonymphidae Koidzumi

Genus Teratonympha Koidzumi (Teranympha K.; Cyclonympha and elongate; transversely ridged, and presents a metameric appearance; each ridge with a single row of fiagella; anterior end complex, containing a nucleus; reproduction by longitudiDogiel). Large
nal fission; in termite gut (Koidzumi, 1917, 1921; Dogiel, 1917).
T. mirabilis

K.

(Fig. 174, g). 200-300/* or longer

by

40-50/*; in Re-

ticulitermes speratus. Mitosis (Cleveland, 1938a).

References

Andrews, Bess

(1930) Method and rate of protozoan refaunation in the termite, etc. Univ. California Publ. Zool., 33:449. Belar, K.: (1926) Der Formwechsel der Protistenkerne. Ergebn. u. Fortschr. Zool., 6:235. Bernstein, T.: (1928) Untersuchungen an Flagellaten aus dem Darmkanal der Termiten aus Turkestan. Arch. Protist., 61:9. Brown, V. E.: (1930) Hypermastigote flagellates from the termites Reticulitermes: etc. Univ. California Publ. Zool., 36:67. (1930a) On the morphology of Spirotrichonympha with a description of two new species, etc. Arch. Protist., 70:517.
J.:

(1931)

The morphology

of

Spironympha,

etc. J.

Morphol.

Phvsiol., 51:291.

HYPERMASTIGINA
:

415

oxygenation and starvation Cleveland, L. R. (1925) on the symbiosis between the termite, Termopsis, and its intestinal flagellates. Biol. Bull., 48:455. (1938) Longitudinal and transverse division in two closely
effects of

The

related flagellates. Ibid., 74:1.

(1938a) Morphology and mitosis of Tetranympha. Arch.

Protist., 91:442.

(1949) The whole life cycle of chromosomes and their coiling systems. Tr. Am. Philos. Soc, 39:1. (1949a) Hormone-induced sexual cycles of flagellates. I. J. Morphol., 85:197. (1950) V. Ibid., 87:349. (1951) VI. Ibid., 88:199. (1951a) VII. Ibid., 88:385. - (1952) VIII. Ibid., 91:269. Hall, S. R., Sanders, E. P. and Collier, Jane: (1934) The wood-feeding roach, Cryptocercus, its Protozoa, etc. Mem. Am. Acad. Arts and Sc., 17:185. Cutler, D. W. (1920) Protozoa parasitic in termites. II. Quart. J. Micr. Sc, 64:383. Dobell, C: (1939) On "Teranympha" and other monstrous latin parasites. Parasitology, 31:255. Dogiel, V. A.: (1917) Cyclonympha strobila n. g., n. sp. J. Microbiol., 4:47. (1922) Untersuchungen an parasitischen Protozoen aus dem Darmkanal der Termiten. II, III. Arch. Soc. Russ. Protist., 1
:

226.

Dropkin, V. H.: (1937) Host-parasite

Protozoa in termites. Univ. California Publ. Zool., 41

(1941) Host ogy, 22:200. (1946) The use of mixed colonies of termites in the study of

relations in the distribution of 189. specificity relations of termite Protozoa. Ecol:

host-symbiont relations.

J. Parasit.,

32:247.

Duboscq, O. and Grasse,

sites

les protistes parades termites de France. V. Arch. zool. exper. gen., 67 (N.-R.):159. (1928a) L'appareil parabasal de Joenia annectens. C. R. Soc. biol., 99:1118. (1943) Les flagelles de V Anacanthotermes ochraccus. Arch. zool. exper. gen., 82:401, and Rose, M.: (1937) La flagelle de V Anacanthotermes ochraceus du Sud-Algerien. C. R. Acad. Sc, 205:574. Grasse, P. P.: (1952) Traite de zoologie. I. Fasc. 1. Paris. and Hollande, A.: (1945) La structure d'une hypermastigine complexe Staurojoenina caulleryi. Ann. Sc. Nat. Bot. Zool., 7:147. Grassi, B.: (1885) Intorno ad alcuni protozoi parassiti delle termiti. Atti Accad. Gioenia Sci. Nat, Catania, Ser. 3, 18:235. (1892) Conclusioni d'una memoria sulla societa dei termiti. Atti R. Accad. Lincei, Ser. 5, 1:33.

P.: (1928)

Notes sur

416

PROTOZOOLOGY

(1917) Flagellati viventi nei termiti. Mem. R. Accad. Lincei, 12:331. and FoA, Anna: (1911) Intorno di protozoi dei termitidi. Atti R. Accad. Lincei, Ser. 5, 20:725. Hungate, R. E.: (1939) Experiments on the nutrition of Zootermopsis. III. Ecology, 20:230. Janicki, C: (1910) Untersuchungen an parasitischen Flagellaten. I. Ztschr. wiss. Zool., 95:245. (1915) II. Ibid., 112:573. Katzin, L. I. and Kirby, H. Jr.: (1939) The relative weights of termites and their Protozoa. J. Parasit., 25:444. Kirby, H. Jr.: (1926) On Staurojoenina assimilis, etc. Univ. California Publ. Zool., 29:25. (1932) Flagellates of the genus Trichonympha. Ibid.,37:349. (1937) Host-parasite relations in the distribution of Protozoa in termites. Ibid., 41:189. (1944) The structural characteristics and nuclear parasites of some species of Trichonympha in termites. Ibid., 49: 185. Kofoid, C. A. and Swezy, Olive: (1919) Studies on the parasites of termites. III. Ibid., 20:41. (1919a) IV. Ibid., 20:99. Koidzumi, M.: (1917) Studies on the Protozoa harboured by the termites of Japan. Rep. Invest, on termites, 6:1. (1921) Studies on the intestinal Protozoa found in the termites of Japan. Parasitology, 13:235. Kudo, R. R.: (1926) Observations on Lophomonas blattaram, etc. Arch. Protist., 53:191. (1926a) A cytological study of Lophomonas striata. Ibid., 55:

504.

Leidy, J.: (1877) On intestinal parasites of Termes flavipes. Proc. Acad. Nat. Sc. Philadelphia, p. 146. Light, S. F.: (1926) Hoplonympha natator. Univ. California Publ. Zool., 29:123. (1927) Kofoidia, a new flagellate, from a California termite. Ibid., 29:467. and Sanford, Mary F.: (1928) Experimental transfaunation of termites. Ibid., 31:269. MacLennan, R. F. and Murer, H. K.: (1934) Localization of mineral ash in the organelles of Trichonympha, etc. J. Morphol., 56:231. Sutherland, J. L.: (1933) Protozoa from Australian termites. Quart. J. Micr. Sc, 76:145. Swezy, Olive: (1923) The pseudopodial method of feeding by trichomonad flagellates parasitic in wood-eating termites. Univ. California Publ. Zool., 20:391.

Chapter

17

Class 2 Sarcodina Hertwig and Lesser

members THE and,

of this class do not possess

any thick

pellicle

therefore, are capable of forming pseudopodia (p. 49).

The term 'amoeboid' is often used to describe their appearance. The pseudopodia serve ordinarily for both locomotion and foodcapturing. The peripheral portion of the body shows no structural
differentiation in

Amoebina, Proteomyxa, and Mycetozoa. Internal

and external

skeletal structures are variously developed in other

and Foraminifera, there is a well-developed test or shell that usually has an aperture, through which the pseudopodia are extruded; in Heliozoa and Radiolaria, skeletons of various forms and materials are developed. The cytoplasm is, as a rule, differentiated into the ectoplasm and the endoplasm, but this differentiation is not constant. In Radiolaria, there is a perforated membranous central capsule which marks the border line between the two cytoplasmic regions. The endoplasm contains the nucleus, food vacuoles and various granules. The majority of Sarcodina are uninucleate, but species of Foraminifera and Mycetozoa are multinucleate in certain phases during their development. In the family Paramoebidae, there occurs a peculiar secondary
orders. Thus, in Testacea

nucleus.

The Sarcodina

are typically holozoic. Their food organisms are

Protozoa, small Metazoa and Protophyta, which present themselves

conspicuously in the cytoplasm.

ready been considered

in parasitic

(p. 97).

The methods One or more

of ingestion

have

al-

contractile vacuoles

are invariably present in forms inhabiting the fresh water, but absent

forms or in those which live in the salt water. Asexual reproduction is usually by binary (or rarely multiple) fission, budding, or plasmotomy. Definite proof of sexual reproduction has been noted in a comparatively small number of species. Encystment is common in the majority of Sarcodina, but is unknown in a few species. The life-cycle has been worked out in some forms and seems to vary among different groups. The young stages are
either

amoeboid or

flagellate,

and on

this account,

it is

sometimes
or

very

difficult to distinguish

the Sarcodina and the Mastigophora.

In some forms the mature trophic stage

flagellate phase,

may show an amoeboid

owing

to differences in environmental conditions.

The Sarcodina

are divided into two subclasses as follows

filopodia
.

With lobopodia, rhizopodia, or With axopodia

Subclass 1 Rhizopoda Subclass 2 Actinopoda

.

(p.

(p.

418) 505)

417

418

PROTOZOOLOGY
Subclass
1

Rhizopoda Siebold

The name Rhizopoda has

class,

often been used to designate the entire

is

but

it is

used here for one of the subclasses, which

further

subdivided into five orders, as follows:

Without test or shell With radiating pseudopodia With rhizopodia; forming Plasmodium. With lobopodia With test or shell
Test single-chambered; chitinous Test 1- to many-chambered; calcareous
.

Order 1 Proteomyxa .Order 2 Mycetozoa (p. 427) Order 3 Amoebina (p. 435)
Order 4 Testacea Order 5 Foraminifera
(p.
(p.

472) 493)

Order

Proteomyxa Lankester

A number
group.

of incompletely

known Rhizopods

are placed in this

The pseudopodia

are filopodia which often branch or anas-

tomose with one another. In this respect the Proteomyxa show affinity to the Mycetozoa. Flagellate swarmers and encystment occur commonly. The majority of Proteomyxa lead parasitic life in algae
or higher plants in fresh or salt water.

Taxonomy (Valkanov,
Family
1

1940).

Pseudoplasmodium-formation Solitary and Heliozoa-like With flagellate swarmers Without flagellate swarmers

Labyrinthulidae
(p. (p.

Family 2 Pseudosporidae Family 3 Vampyrellidae

420) 420)

Family

Labyrinthulidae Haeckel

Small fusiform protoplasmic masses are grouped in network of sparingly branched and anastomosing filopodia; individuals encyst independently; with or without flagellate stages. Genus Labyrinthula Cienkowski. Minute forms feeding on various
species of algae in fresh or salt water; often brightly colored
carotin. Jepps (1931)

found these organisms

varieties, while

common

in

due to marine

aquaria.

Young

(1943) considers the six

three species and

two

known species as actually Watson (1951) holds that only

one species, L. macrocystis, should be recognized. L. cienkowskii Zopf (Fig. 176, a). Attacks Vaucheria in fresh water. L. macrocystis Cienkowski. Renn (1934, 1936) found a species in the diseased leaf-tissue of the 'spotting and darkening' eel-grass, Zostera marina, along the Atlantic coast of the United States. Young (1943) identified the organism which he studied as L. macrocystis, and noted that its hosts included various algae and three genera of Naiadaceae: Zostera, Ruppia and Zannichellia. The 'net-plasmodium' contains fusiform cells which average in size

SARCODINA, PROTEOMYXA

419

18/x by 4/x and which multiply by binary fission; many cells encyst together within a tough, opaque membrane. The growth is best at 14-24C. and at 12-22 per cent chlorinity (Young). Watson and Ordal (1951) cultivated the organism on agar and sea water with various bacteria, and found that the organism is fusiform in youngcultures; highly motile; filamentous projections are formed from the flat mucoid lamellae, secreted by the organism, and expand to form passways over which the organism travels; holozoic, saprozoic. Genus Labyrinthomyxa Duboscq. Body fusiform; amoeboid and

flagellate phases, variable in size; flagellate stage penetrates the host

cell

membrane;

in plants.

Fig. 176. a, Labyrinthula cienkowskii, X200 (Doflein); b-e, Labyrinthomyxa sauvageaui (b, c, flagellate forms, XlOO; d, e, amoeboid forms, X500) (Duboscq); f, g, Pseudospora volvocis, X670 (Robertson); h-j, Protonwnas amyli (Zopf);k, 1, Vampyrella lateritia, X530 (k (Leidy), 1 (Doflein)); m, n, Nuclearia delicatula, X300 (Cash).

420

PROTOZOOLOGY

L. sauvageaui D. (Fig. 176, b-e). Fusiform body 7 llyu long; pseudoplasmodium-formation; amoeboid stage 2.5-14ju long; flagellate stage 7-18/z long; parasitic in Laminaria lejolisii at Roscoff, France.

Family 2 Pseudosporidae Berlese

Genus Pseudospora Cienkowski. Body minute; parasitic in algae and Mastigophora (including Volvocidae) organism nourishes itself on host protoplasm, grows and multiplies into a number of smaller individuals, by repeated division; the latter biflagellate, seek a new host, and transform themselves into amoeboid stage; encystment common. Morphology and development (Schussnig, 1929).
;

P. volvocis C. (Fig. 176,

species of Volvox.

/,

g).

diameter; pseudopodia radiating; cysts about

P. -parasitica C.

Heliozoan form about 12-30/1 25ju in diameter;

algae.

in in

Morphology (Roskin, 1927). Attacks Spirogyra and allied

P. eudorini Roskin. Heliozoan forms 10-12/x in diameter; radiating pseudopodia 2-3 times longer; amoeboid within host colony; cysts
15 n in diameter; in Eudorina elegans.
irregularly rounded with food consists of starch grains; division into biflagellate organisms which become amoeboid and unite to form

Genus Protomonas Cienkowski. Body

filo podia;

radiating

pseudo plasmodium; fresh or salt water. P. amyli C. (Fig. 176, h-j). In fresh water.

Family 3 Vampyrellidae Doflein

Filo podia radiate
flagellate

from

all sides

or formed from a limited area;

the organism

is able to bore through the cellulose membrane of various algae and feeds on protoplasmic contents; body often reddish because of the presence of carotin; multinucleate; multiplication in encysted stage into uni- or

forms do

not occur;

multi-nucleate bodies; cysts often also reddish.

Genus Vampyrella Cienkowski. Heliozoa-like; endoplasm vacuowith carotin granules; numerous vesicular nuclei and contractile vacuoles; multinucleate cysts, sometimes
lated or granulated,

with stalk; 50-700/* in diameter. Several species.

V. lateritia (Fresenius) (Fig. 176, k, I). Spherical; orange-red except the hyaline ectoplasm; feeds on Spirogyra and other algae in fresh water. On coming in contact with an alga, it often travels

along

it and sometimes breaks it at joints, or pierces individual cell and extracts chlorophyll bodies by means of pseudopodia; multipli-

cation in encysted condition; 30-40/z in diameter. Behavior (Lloyd,

1926, 1929).

SARCODINA, PROTEOMYXA

421

Genus Nuclearia Cienkowski. Subspherical, with sharply pointed fine radiating pseudopodia; actively moving forms vary in shape; with or without a mucous envelope; with one or many nuclei; fresh
water.

Fig. 177. a, Arachnula impatiens, X670 (Dobell); b, c, Chalnwjdomyxa montana: b, X270 (Cash); c, X530 (Penard); d, Rhizoplasma kaiseri, (Verworn); e, Biomyxa vagans, X200 (Cash); f, Penardia mutabilis, X200

(Cash);

g,

Hyalodiscus rubicundus, X370 (Penard).

422

PROTOZOOLOGY
delicatula C. (Fig. 176,

N.

m,

n).

Multinucleate; bacteria often

adhering to gelatinous envelope; up to 60m in diameter. N. simplex C. Uninucleate 30ju in diameter. Genus Arachnula Cienkowski. Body irregularly chain-form with
;

filo podia

contractile vacuoles; feeds

extending from ends of branches; numerous nuclei and on diatoms and other microorganisms.
a).

A. impatiens C. (Fig. 177,

40-35Gy

in diameter.

Genus Chlamydomyxa Archer. Body spheroidal; ectoplasm and endoplasm well differentiated; endoplasm often green-colored due to the presence of green spherules; numerous vesicular nuclei; 1-2 contractile vacuoles; secretion of an envelope around the body is followed by multiplication into numerous secondary cysts; cyst wall cellulose; in sphagnum swamp. C. montana Lankester (Fig. 177, b, c). Rounded or ovoid; cytoplasm colored; about 50/* in diameter; when moving, elongate with extremely fine pseudo podia which are straight or slightly curved and which are capable of movement from side to side; non-contractile vacuoles at bases of grouped pseudo pods; in active individual there is a constant movement of minute fusiform bodies (function?); when extended 100-150^ long; total length 300/x or
more; fresh water among vegetation. Genus Rhizoplasma Verworn. Spherical or sausage-shaped; with anastomosing filo podia; orange-red; with a few nuclei. R. kaiseri V. (Fig. 177, d). Contracted form 0.5-1 mm. in diameter; with 1-3 nuclei; pseudo podia up to 3 cm. long; extended body up to 10 mm. long; originally described from Red Sea.

Genus Chondropus

Greeff. Spherical to oval; peripheral portion

filled

transparent but often yellowish; endoplasm

with green, yellow,

brown bodies; neither nucleus nor

contractile vacuoles observed;

pseudo pods straight, fine, often branched; small pearl-like bodies on body surface and pseudopodia. C. viridis G. Average diameter 35-45^; fresh water among algae. Genus Biomyxa Leidy (Gymnophrys Cienkowski). Body form inconstant; initial form spherical; cytoplasm colorless, finely granulated, capable of expanding and extending in any direction, with many filopodia which freely branch and anastomose; cytoplasmic

movement
in

active throughout; numerous small contractile vacuoles body and pseudopodia; with one or more nuclei.

size varies greatly; in

e). Main part of body, of various forms; sphagnous swamps, bog-water, etc. B. cometa (C). Subspherical or irregularly ellipsoidal; pseudopodia small in number, formed from 2 or more points; body 35-40/z, or up

B. vagans L. (Fig. 177,

SARCODINA, PROTEOMYXA
to 80/x or

423

more; pseudopodia

400/x long or longer.

Cienkowski main-

tained that this was a moneran.

Genus Penardia Cash. When inactive, rounded or ovoid; at other times expanded; exceedingly mobile; endoplasm chlorophyll-green with a pale marginal zone; filopodia, branching and anastomosing,
colorless; nucleus inconspicuous;

one or more contractile vacuoles,

small; fresh water.

P. mutabilis C. (Fig. 177, /). Resting form 90-100/x in diameter; extended forms (including pseudopodia) 300-400/x long. Genus Hyalodiscus Hertwig and Lesser. Discoid, though outline
varies;

endoplasm reddish, often vacuolated and sometimes shows

filamentous projections reaching body surface; a single nucleus;

ectoplasmic band of varying width surrounds the body completely;

closely allied to Vampyrella; fresh water.

H. rubicundus H. and L. (Fig. 177, g). 50-80/x by about 30ju; polymorphic; when its progress during movement is interrupted by
an object, the body doubles back upon itself, and moves on in some other direction; freshwater ponds among surface vegetation. Genus Leptomyxa Goodey. Multinucleate, thin, amoeboid organisms; multinucleate cysts formed by condensation of protoplasm;
free-living in soil

(Goodey, 1915).
(Fig. 178, a-c).

L. reticulata

G.

Body composed

of a thin trans-

parent protoplasm;

when

fully extended, 3

mm.

or

more

in length;

superficially resembles

an endosporous mycetozoan, but no reversible cytoplasmic movement; multinucleate with eight to 20 to several hundred nuclei; nuclei, 5-6/z in diameter, with a large endosome; nuclear division simultaneous, but not synchronous; plasmotomy;

local condensation of protoplasm; widely distributed in British soil (Singh, 1948, 1948a). McLennan (1930) found a similar organism in and on the root of diseased hops in Tasmania.

plasmogamy; cysts multinucleate, by

Genus Megamoebomyxa Nyholm. Extremely

large

amoeboid

or-

ganism; when contracted, lobulate, with adhering detritus; when cultured at 8-10C. on debris, filopodia are formed and form-change occurs; lobate during locomotion; "nutrient chiefly detritus"; Ma-

(Nyholm, 1950). N. (Fig. 178, d). An opaque white organism; up to 25 mm. long; polymorphic; in marine sediment, rich in debris at the depth of 45-70 in.; Gullmar Fjord, Sweden. Genus Reticulomyxa Nauss. Highly polymorphic, multinucleate amoeboid organism; rhizopodia radiating from a central mass of undifferentiated granular protoplasm with many non-contractile vacurine.

One

species

M.

argillobia

424

PROTOZOOLOGY

b,

Fig. 178. a-c, Leptomyxa reticulata, X73 (Singh) (a, a trophozoite; cyst-formation; c, a cyst); d, an individual of Megamoebomyxa argile,

lobia,

showing the changes of body form, X2/3 fNyholm); trophozoite of Reticulomyxa filosa, X3 (Nauss).

a young

oles;

particles

plasmotomy usually into three, after discarding extraneous and migrating to new site; when transferred to fresh dish of

water, "spore-like" bodies are dispersed; fresh water

leaves.

among decaying
Myceto-

Nauss (1949) points out zoa and Foraminifera.

its affinity

to Proteomyxa,

is

R. filosa N. (Fig. 178, e). On moist blotting paper the central mass an elevated body, but in water it spreads into a broad sheet, 4-6 mm. in diameter; pseudopodia may be up to 10 times the diameter

of the central white

mass; encyst ment occurs when subjected to

SARCODINA, PROTEOMYXA
lower temperature or

425

when

cultured with algae; food consists of

debris.

"worms,"

rotifers

and organic

References

Cash,

and Wailes, G. H. (1915-1918) 3, 4 London. Doflein, F. and Reichenow, E.: (1929) Lehrbuch der Protozoen:

(1905,1909) The Heliozoa. 1, 2. London.

J.:

British

freshwater

Rhizopoda

and

kunde. 5 ed. Jena. A.: (1926) Morphologie der Tiere in Bildern. H.2, T.2. Rhizopoden. Jena. Leidy, J.: (1879) Freshwater Rhizopods of North America. Rep. U. S. Geol. Survey, 12. Penard, E.: (1902) Faune rhizopodique du bassin du Leman. Geneva.

Kuhn,

Cash, J.: (1905) The British freshwater Rhizopoda and Heliozoa. 1. London. Cienkowski, L.: (1863) Das Plasmodium. Pringsheim's Jahrb. Bot.,
3:400. (1867) Ueber den Bau und die Entwicklung der LabyrinthuArch. mikr. Anat., 3:274. leen. Dobell, C: (1913) Observations on the life-history of Cienkowski's Arachnula. Arch. Protist., 31:317. Duboscq, O.: (1921) Labyrinthomyxa sauvageaui, etc. C. R. Soc. bid., 84:27. Goodey, T.: (1915) A preliminary communication of three new proteomyxan rhizopods from soil. Arch. Protist., 35:80. Jepps, Margaret W.: (1931) Note on a marine Labyrinthula. J. Marine Biol. Ass. United Kingdom, 17:833. Lloyd, F. E.: (1926) Some behaviours of Vampyrella lateritia, etc. Papers Mich. Acad. Sc, 6:275. (1929) The behavior of Vampyrella lateritia, etc. Arch. Protist., 67:219. McLennan, E. I.: (1930) A disease of hops in Tasmania and an account of a proteomyxan organism, etc. Australian J. Exper.
Biol., 7:9.

Nauss, Ruth N.: (1949) Reticulomyxa filosa,

Club, 76:161. Nyholm, K.-G.: (1950)

etc. Bull.

Torrey Bot.

marine nude rhizopod type Megamoebo-

myxa Renn, C.

argillobia.

E.: (1935)

Zool. Bidrag. Uppsala, 29:93. mycetozoan parasite of Zostera marina.

Na-

ture, 135:544.

(1936) The wasting disease of Zostera marina. Biol. Bull., 70:148. Roskin, G.: (1927) Zur Kenntnis der Gattung Pseudospora. Arch. Protist., 59:350. Schussnig, B.: (1929) Beitrage zur Entwicklungsgeschichte der Protophyten. IV. Ibid., 68:555.

426

PROTOZOOLOGY
I. J.

Singh, B. N.: (1948) Studies on giant amoeboid organisms.

Gen.

Microbiol., 2:7. (1948a) II. Ibid., 2:89. Valkanov, A.: (1929) Protistenstudien. IV. Arch. Protist., 67:110. (1940) Die Heliozoen und Proteomyxien. Ibid., 93:225. Watson, S. W. and Ordal, E. J.: (1951) Studies on Labyrinthula. Univ. Washington Oceanogr. Lab., Tech. Rep., 3, 37 pp. Young, E. L.: (1943) Studies on Labyrinthula, etc. Am. J. Bot., 30: 586. Zopf, W.: (1887) Handbuch der Botanik (A. Schenk), 3:24.

Chapter

18

Order 2 Mycetozoa de Bary

be had been considered THE Mycetozoa Myxomycetes, or being known
to
fungi,

closely related to the

as

Myxogasteres, the

Through extended studies de Bary showed that they are more closely
'slime

molds.'

of their development,

related to the Protozoa than to the Protophyta, although they stand undoubtedly on the border-line between these two groups of microorganisms. The Mycetozoa occur on dead wood or decaying vegetable matter of various
kinds.

The most conspicuous part of a mycetozoan is its Plasmodium is formed by fusion of many myxamoebae, thus producing a large multinucleate body (Fig. 179, a). The greater part of the
which

cytoplasm is granulated, although there is a thin layer of hyaline and homogeneous cytoplasm surrounding the whole body. The numerous
vesicular nuclei are distributed throughout the granular cytoplasm.

Many
as the

small contractile vacuoles are present in the peripheral por-

Plasmodium. The nuclei increase in number by division division seems to be amitotic during the growth period of the Plasmodium, but is mitotic prior to the sporeformation. The granulation of the cytoplasm is due to the presence of enormous numbers of granules which in some forms are made up of carbonate of lime. The Plasmodium is usually colorless, but sometimes yellow, green, or reddish, because of the numerous droplets of fluid pigment present in the cytoplasm.
tion of the

body grows; the

The food of Mycetozoa varies among different species. The great majority feed on decaying vegetable matter, but some, such as Badhamia, devour living fungi. Thus the Mycetozoa are holozoic or
saprozoic in their

mode of nutrition. Pepsin has been found in the Plasmodium of Fuligo and is perhaps secreted into the food vacuoles, into which protein materials are taken. The Plasmodium of Badhamia is said to possess the power of cellulose digestion.

When

exposed to unfavorable conditions, such as desiccation,

the protoplasmic

movement

ceases gradually, foreign bodies are

extruded, and the whole Plasmodium becomes divided into numerous sclerotia or cysts, each containing 10-20 nuclei and being sur-

rounded by a resistant wall

years.

(6).

These cysts

may live as long

as three

Upon

return of favorable conditions, the contents of the

sclerotia germinate, fuse together,

(c-e).

and thus again produce plasmodia

When

lack of food material occurs, the

Plasmodium undergoes

427

428

PROTOZOOLOGY

changes and develops sporangia. The first indication of this process is the appearance of lobular masses of protoplasm in various parts of the body (/, g). These masses are at first connected with the streaming protoplasmic thickenings, but later become completely segregated into young sporangia. During the course of sporangium-formation, foreign bodies are thrown out of the body, and around each

179. The life-cycle of the endosporous mycetozoan (de Bary, and others), a, plasmodium-formation by fusion of numerous myxamoebae; b, c, formation of sclerotium; d, e, germination of sclerotium and formation of Plasmodium; f, portion of a Plasmodium showing

Fig.

Lister,

streaming protoplasmic thickenings; g, h, formation of sporangia; i, a sporangium opened, showing capillitium; j, a spore; k, germination of
spore; 1, myxamoeba; m, n, myxoflagellates; o-q, multiplication of myxoflagellate; r, microcyst; s, myxamoeba. Variously magnified.

sporangium there is secreted a wall which, when mature, possesses a wrinkled appearance (h). The wall continues down to the substratum as a slender stalk of varying length, and in many genera the end of a stalk spreads into a network over the substratum, which forms the base, hypothallus, for the stalk. With these changes the interior

MYCETOZOA
of the
capillitium, of flat

429

sporangium becomes penetrated by an anastomosing network, bands which are continuous with the outer covering (i). Soon after the differentiation of these protective and supporting structures, the nuclei divide simultaneously by mitosis and the cytoplasm breaks up into many small bodies. These uninucleate bodies are the spores which measure 3-20/x in diameter and which
soon become covered by a more or
less thick cellulose

membrane

(j),

variously colored in different species.

The mature sporangium breaks open sooner or later and the by the wind. When a spore falls in water, its membrane ruptures, and the protoplasmic contents emerge as an amoebula (k, I). The amoebula possesses a single vesicspores are carried, and scattered,
ular nucleus

and contractile vacuoles, and undergoes a typical amoe-

boid movement. It presently assumes an elongate form and one flagellum or two unequally long flagella (Elliott, 1948) develop from the nucleated end, thus forming a myxoflagellate (m, n) which under-

movement and is able to form short, pointed pseudopodia from the posterior end. It feeds on bacteria, grows and multiplies by binary fission (o-q). After a series of division, the myxogoes a peculiar dancing
flagellate

may

encyst and becomes a microcyst

(r).

When

the micro(s)

cyst germinates, the content develops into a

myxamoeba

which,

through fusion with many others, produces the Plasmodium mentioned above. This is the life-cycle of a typical endosporous mycetozoan.
face of sporophores, the development

In the genus Ceratiomyxa in which spores are formed on the suris briefly as follows: the
lives

Plasmodium
appearance.

on or
is

in

The body

decayed wood and presents a horn-like covered by a gelatinous hyaline substance,

within which the protoplasmic movements

may be noted. The protoplasm soon leaves the interior and accumulates at the surf ace of the mass; at first as a close-set reticulum and then into a mosaic of
polygonal

moves outward

each containing a single nucleus. Each of these cells at right angles to the surface, still enveloped by the thin hyaline layer, which forms a stalk below. These cells are spores which become ellipsoid and covered by a membrane when fully formed. The spore is uninucleate at first, but soon becomes tetranucleate. When a spore reaches the water, its content emerges as an amoebula which divides three times, forming 8 small bodies, each
cells,

of

which develops a flagellum and becomes a myxoflagellate. The remaining part of the development is presumably similar to that of the endosporous form. Morphology (de Bary, 1864, 1884; MacBride, 1922; Jahn, 1928; MacBride and Martin, 1934).

430

PROTOZOOLOGY
large

number

of

(Hagelstein, 1944).

The order

mycetozoan genera and species are known is divided here into two suborders.

Spore develops into myxoflagellate; myxamoebae fuse completely and form Plasmodium Suborder 1 Eumycetozoa No flagellate stage; myxamoebae grouped prior to spore-formation, but do not fuse to form a true Plasmodium Suborder 2 Sorophora (p. 433)

Suborder

Eumycetozoa Zopf

Spores develop within sporangia Spores violet or violet-brown Sporangia with lime Lime in small granular form

Family

Physaridae

X4;

Fig. 180. a, b, Badhamia utricularis Berkeley (a, cluster of sporangia, b, part of capillitium and spore-cluster, X140) (Lister); c, d, Fuligo

Gmelin (c, a group of sporangia, X^; d, part of capillitium and two spores, X120) (Lister); e, f, Didymium effusum Link (e, sporangium, Xl2; f, portion of capillitium and wall of sporangium showing the crystals of calcium carbonate and two spores, X200) (Lister); g, h, Stemonitis splendens Rostafinski (g, three sporangia, X2; h, columella and capillitium, X42) (Lister).
septica

Genus Badhamia Berkeley

(Fig.

180, a, b)

Capillitium, a course network with lime throughout.

Genus Fuligo Haller

sions filled with granules of lime.

(Fig.

180,

c,

d)

Capillitium, a delicate network of threads with vesicular expan-

Lime

in crystalline

form

Family 2 Didymiidae

MYCETOZOA
Genus Didymium Schrader
Lime
Sporangia without lime Sporangia stalked
(Fig. 180,
e,

431
f)

crystals stellate, distributed over the wall of sporangium.

Family 3 Stemonitidae
(Fig. 180, g, h)
all

Genus Stemonitis Gleditsch

Sporangium-wall evanescent; capillitium arising from columella to form a network.

Sporangium combined
into aethalium

parts of

Family 4 Amaurochaetidae

Genus Amaurochaete Rostafinski

With

(Fig. 181,

a,

b)

irregularly branching thread-like capillitium.

Spores variously colored, except violet Capillitium absent or not forming a system of uniform threads. Sporangium-wall membranous; with minute round granules

Family 5 Cribrariidae

c^ggfc,

W$9

f?m

angia,

Amaurochaete fuliginosa MacBride (a, group of sporXlO) (Lister); c, empty sporangium of Cribraria aurantiaca Schrader, X20 (Lister); d, sporangium of Orcadella operculata Wingate, X80 (Lister); e, cluster of sporangia of Tubulina fragiformis Persoon, X3 (Lister); f, aethalium of Reticularia lycoperdon Bull., XI (Lister); g, aethalium of Lycogala miniatum Persoon Xl (Lister); h-j, Trichia affinis de Bary (h, group of sporangia, X2; i, elater, X250; j, spore, X400) (Lister); k, 1, Arcyria punicea Persoon (k, four sporangia, X2; 1, part of capillitium, X 250 and a spore, X 560) (Lister); m, n, Ceratiomyxa fruticulosa MacBride (m, sporophore, X40; n, part of mature sporophore, showing two spores, X480) (Lister).
Fig. 181.
a, b,

X;

b, capillitium,

432

PROTOZOOLOGY
Genus Cribraria Persoon
(Fig. 181, c)

Sporangia stalked; wall thickened and forms a delicate persistent network expanded at the nodes.
Sporangia solitary; stalked

Family 6 Liceidae
(Fig. 181, d)

Genus Orcadella Wingate

Sporangia stalked, furnished with a

lid of

thinner substance.

Sporangium-wall membranous without granular deposits Family 7 Tubulinidae

Genus Tubulina Persoon

Sporangia without tubular extensions.

(Fig. 181, e)

Many

(aethalia); sporangium-wall incomplete

sporangia more or less closely fused to form large bodies and perforated

Family 8 Reticulariidae

Genus Reticularia Bulliard

(Fig. 181,/)

Walls of convoluted sporangia incomplete, forming tubes and folds with numerous anastomosing threads.
Sporangia forming aethalium

Family 9 Lycogalidae
(Fig. 181, g)

Genus Lycogala Micheli

Oapillitium a system of uniform threads Capillitium threads with spiral or annular thickenings Family 10 Trichiidae

Genus Trichia Haller

Capillitium
thickenings.

(Fig. 181, h-j)

abundant,

consisting

of

free

elasters

with spiral

Capillitium combined into an elastic network with thickenings in forms of cogs, half-rings, spines, or warts. Family 11 Arcyriidae

Genus Arcyria Wiggers

(Fig. 181,

A;,

I)

Sporangia stalked; sporangium-wall evanescent above, persistent and membranous in the lower third.
Capillitium abundant; sporangia normally sessile Family 12 Margaritidae

Genus Margarita

Lister

Capillitium profuse, long, coiled hair-like.

Spores develop on the surface of sporophores Spores white; borne singly on filiform stalk

Family 13 Ceratiomyxidae

MYCETOZOA
Genus Ceratiomyxa Schroter
(Fig. 181,

433

m, n)

Suborder 2 Sorophora Lister

Pseudoplasmodium incomplete; myxamoeba
of

limax-form

Family 1 Guttuliniidae Pseudoplasmodium complete; myxamoeba with short pointed pseudoFamily 2 Dictyosteliidae podia

The Proteomyxa and

the Mycetozoa as outlined above, are not

line

distinctly defined groups. In reality, there are a

which stand on the border

number of forms between them. Development of Dictyostelium discoideum (Raper, 1940) food habits and distribution
;

of Dictyostelium (Singh, 1947, 1947a).

Phytomyxinea Poche
These organisms which possess a large multinucleate amoeboid body, are parasitic in various plants and also in a few animals. Taxonomy (Palm and Burk, 1933; Cook, 1933). Genus Plasmodiophora Woronin. Parasitic in the roots of cabbage and other cruciferous plants. The organism produces knotty enlargements, sometimes known as "root-hernia," or "fingers and toes" (Fig. 182, a). The small (haploid) spore (6) gives rise to a myxoflagellate (c-f) which penetrates the host cell. The organism grows in size

6
#&$

spore,
h,

Fig. 182. Plasmodiophora brassicae. a, root-hernia of cabbage; b, a X620; c-e, stages in germination of spore, X620; f, myxamoeba, X620 (Woronin); g, a host cell with several young parasites, X400;

an older

parasite,

X400 (Nawaschin).

and multiplies (g, h). The Plasmodium divides into sporangia. Flagellated gametes that develop from them fuse in pairs, giving rise to diploid zygotes. These zygotes develop further into plasmodia in which haploid spores are produced. Morphology (Jones, 1928) cy;

tology (Milovidov, 1931).

P. brassicae

W.

(Fig. 182).

In Brassica spp.

434

PROTOZOOLOGY
Sorosphaera Schroter. Parasitic in Veronica spp.

Genus Genus Genus Genus Genus Genus

dubia.

Tetramyxa Goebel. In Ruppia, Zannichellia, etc. Octomyxa Couch, Leitner and Whiffen. In Achlya glomerata. Sorodiscus Lagerheim and Winge. In Chara, Callitriche, etc. Polymyxa Ledingham. In Triticum, etc. Membranosorus Ostenfeld and Petersen. In Heteranthera
Parasitic in
as

Genus Spongospora Brunchorst.

eased condition of potatoes
is

known

Solanum; the powdery or corky scab.

etc.

dis-

Genus Ligniera Maire and Tison. In Alisma, Juncus,

References

Cook, W. R.

I.:

(1933)

monograph

of the Plasmodiophorales.

Arch. Protist., 80:179.

de Bary, A.: (1864) Die Mycetozoa. Leipzig. (1884) Vergleichende Morphologie und Biologie der Pilze, Mycetozoen, und Bacterien. Leipzig. Elliott, E. W.: (1948) The sperm-cells of Myxomycetes. J. Washof North America. New York. Jahn, E.: (1901-1920) Myxomycetenstudien. I-X. Ber. deutsch. bot. Ges., 19, 20, 22-26, 29, 36 and 37. - (1928) Myxomycetenstudien. XII. Ibid., p. 80. Jones, P. M.: (1928) Morphology and cultural study of Plasmodiophora brassicae. Arch. Protist., 62:313. Karling, J. S.: (1942) The Plasmodiophorales. New York. Lister, A.: (1925) A monograph on the Mycetozoa. 3 ed. London. MacBride, T. H.: (1922) North American slime molds. 2 ed. New York. and Martin, G. H.: (1934) The Myxomycetes. New York. Milovidov, P. F.: (1931) Cytologische Untersuchungen an Plasmodiophora brassicae. Arch. Protist., 73:1. Palm, B. T. and Burk, Myrle: (1933) The taxonomy of the Plasmodiophoraceae. Ibid., 79:262. Raper, K. B.: (1940) Pseudoplasmodium formation and organization in Dictyostelium discoideum. J. Elisha Mitchell Sc. Soc,

ington Acad. Sc, 38:133. Hagelstein, R.: (1944) The Mycetozoa

56:241.

Singh, B. N.: (1947) Studies on soilAcrasieae.

1:11.

I.

J.

Gen. Microbiol.,

(1947a)

II. Ibid.,

1:361.

Chapter

19

Order 3 Amoebina Ehrenberg

There Amoebina show a very THE surrounding the body, although no thick
little cortical differentiation.
is

pellicle or test,

in

some a

delicate pellicle occurs.

The cytoplasm

is

more

or less dis-

and the endoplasm. The ectoplasm is hyaline and homogeneous, and appears tougher than the endoplasm. In the endoplasm, which is granulated or vacuolated, are found one or more nuclei, various food vacuoles, crystals, and other inclusions. In the freshwater forms, there is at least one distinctly
tinctly differentiated into the ectoplasm
visible contractile vacuole.

The pseudopodia

are lobopodia,
in

and

ordi-

them. They are formed by streaming or fountain movement of the cytoplasm. In some members of this order, the formation of pseudopodia is eruptive or explosive, since the granules present in the endoplasm break through the border line between the two cytoplasmic layers and
narily both the ectoplasm

and endoplasm are found

suddenly flow into the pseudopodia. Asexual reproduction is ordinarily by binary fission, although multiple fission may occasionally take place. Encystment is of common occurrence. Sexual reproduction, which has been reported in a few species, has not been confirmed.

The Amoebina inhabit all sorts of fresh, brackish, and salt waters. They are also found in moist soil and on ground covered with decaying leaves.

Many

are inhabitants of the digestive tract of various status of the group

animals, and some are pathogenic to the hosts.

The taxonomic

is

highly uncertain and con-

mostly unknown and since numerous protozoans other than the members of this group often possess amoeboid stages. The order is subdivided into four families as follows:
fusing, since their life-histories are

With amoeboid and

flagellate stages

Family

Naegleriidae

Amoeboid stage only With one or more nuclei

Free-living
Parasitic

of

one kind

With a secondary nucleus

Family 2 Amoebidae Family 3 Endamoebidae Family 4 Paramoebidae

1

(p.
(p. (p.

437) 443) 405)

Family

Naegleriidae
in this family possess

The members
amoeboid and

of the

two genera placed

both

flagellate phases [diphasic).

In the former, the organ-

435

436

PROTOZOOLOGY

ism undergoes amoeboid movement by means of lobopodia and in the latter the body is more or less elongated. Binary fission seems to take place during the amoeboid phase only. Thus these are diphasic amoebae, in which the amoeboid stage predominates over the flagellate. The amoeboid phase is often a 'limax' form; under natural
it is often exceedingly difficult by observing the amoeboid stage only, to determine whether they belong to this family or the family Amoebidae. Genus Naegleria Alexeieff. Minute flagellate stage with 2 flagella; amoeboid stage resembles Vahlkampfia (p. 442), with lobopodia; cytoplasm differentiated; vesicular nucleus with a large endosome;

circumstances,

contractile vacuole conspicuous; food vacuoles contain bacteria;

cysts uninucleate; free-living in stagnant water and often coprozoic.

Taxonomy and

cytology (Rafalko, 1947; Singh, 1952).

Fig. 183. a-c, trophozoite, flagellate phase and cyst Call stained) of Naegleria gruberi, X750 (Alexeieff); d-f, similar stages of N. bistadialis, X750 (Kiihn); g-j, trophozoite, flagellate phase, cyst, and excystment of

Trimastigamoeba philippinensis, X950 (Whitmore).

N. gruberi (Schardinger) (Fig. 183, a-c). Amoeboid stage 10 36jtt by 8-18/*; cyst uninucleate; cyst wall with several apertures; flagellate stage 18/x by 8/t; stagnant water and often coprozoic. N. bistadialis (Puschkarew) (Fig. 183, d-f). Similar in size; but cyst with a smooth wall. Genus Trimastigamoeba Whitmore. Flagellate stage bears 3
equal length vesicular nucleus with a large endosome; amoeboid stage small, less than 20/x in diameter; uninucleate cysts with smooth wall stagnant water.
flagella of nearly
; ;

T. philippinensis

W.

(Fig. 183, g-j).

Amoeboid stage

16-18/x in

diameter; oval cysts 13-14/x

6-8m.

by

8-12/t; flagellate stage 16-22/t

by

AMOEBINA
Family 2 Amoebidae Bronn

437

These amoebae do not have flagellate stage and are exclusively amoeboid (monophasic) They are free-living in fresh or salt water, in damp soil, moss, etc., and a few parasitic; 1, 2, or many nuclei;
.

contractile vacuoles in freshwater forms; multiplication

by binary

or multiple fission or

plasmotomy: encystment common. Genera

Miiller;

(Leidy, 1879; Penard, 1902; Singh, 1952).

Genus Amoeba Ehrenberg (Proteus

boid; a vesicular nucleus, either with

Amiba Bory). Amoegranules or with

many spherical

a conspicuous endosome; usually one contractile vacuole; pseudopodia are lobopodia, never anastomosing with one another; holozoic;
in fresh, brackish or salt water.

(SchaefTer, 1926;

Numerous species. Nomenclature Mast and Johnson, 1931; Kudo, 1952).

2, e, f;

A. proteus (Pallas) (Figs.

a, b).

25; 33,

b, c;

43,/; 45-47; 68; 184,

600m or longer in largest diameter; creeping with a few large lobopodia, showing longitudinal ridges; ectoplasm and endoplasm usually distinctly differentiated; typically uninucleate; nucleus discoidal but polymorphic; endoplasmic crystals truncate bipyramid, up to 4.5m long (SchaefTer, 1916); nuclear and cytosomic divisions show a distinct correlation (p. 169); fresh water. Cytology (Mast, 1926; Mast and Doyle, 1935, 1935a) nuclear division (Chalkto
;

Up

ley, 1936; Liesche, 1938).

A. discoides SchaefTer (Figs. 43, g; 184, c). About 400m long during locomotion; a few blunt, smooth pseudo podia; crystals abundant, truncate bipyramidal, about 2.5m long (SchaefTer) endoplasm with
;

numerous coarse granules;

fresh water.

A. dubia S. (Figs. 43, h-l; 184, d). About 400m long; numerous pseudo podia flattened and with smooth surface; crystals, few, large, up to 30m long and of various forms among which at least 4 types are said to be distinct (SchaefTer); contractile vacuole one or

more; fresh water. Nuclear division (Dawson et al., 1935); viscosity (Angerer, 1942); contractile vacuole (Dawson, 1945). A. verrucosa Ehrenberg (Figs. 33, a, d-h; 44, a; 184, e). Ovoid in general outline with wart-like expansions; body surface usually wrinkled, with a definite pellicle; pseud opodia short, broad and blunt, very slowly formed; nucleus ovoid, vesicular, with a large endosome; contractile vacuole; up to 200m in diameter; fresh water

among
A.

algae.

Penard (Fig. 184,/). Somewhat similar to A. verrucosa, but small; body flattened; ovoid, narrowed and rounded posteriorly; nucleus vesicular; contractile vacuole comparatively large and often
striata

438

PROTOZOOLOGY

not spherical; extremely delicate pellicle shows 3 or 4 fine longitudinal lines which appear and disappear with the movement of the body; 25-45/z by 20-35ju; fresh water among vegetation.

Fig. 184.
c,

a, b,

Amoeba

proteus

(a,

X130

(Schaeffer), b, cyst (Doflein));

A. discoides, X130 (Schaeffer); d, A. dubia, X130 (Schaeffer); e, A. verrucosa, X200 (Cash); f, A. striata, X400 (Penard); g, A. guttula, X800 (Penard); h, A. limicola, X530 (Penard).

A. guttula Dujardin (Fig. 184, g). Ovoid during locomotion, narrowed posteriorly and often with a few minute, nipple-like dentations; movement by wave-like expansions of ectoplasm; endoplasm
granulated, with crystals; nucleus vesicular; a single contractile vacuole; 30-35/z

by

20-25)u; fresh water in vegetation.

h).

A. limicola Rhumbler (Fig. 184,

Somewhat

similar to A. gut-

AMOEBINA
tula;

439

body more rounded; locomotion by eruption of cytoplasm through the body surface; 45-55/z by 35/x; nucleus vesicular; fresh
water among vegetation.

Fig. 185. a, Amoeba spumosa, X400 (Penard); X300 (Penard); d-f, A. gorgonia, X400 (Penard); (Penard); h, Dinamoeba mirabilis, X250 (Leidy).

b,
g,

c, A. vespertilio, A. radiosa, X500

A. spumosa Gruber (Fig.

2, c,

d; 185, a).

Somewhat fan-shaped;

flattened; during locomotion broad pseudopodia with pointed end;

temporary posterior region with nipple-like projections; a small

440

PROTOZOOLOGY
of striae
pellicle;

number
is

a very thin

varying in size

become visible during movement, showing there endoplasm always vacuolated, the vacuoles (up to 30m in diameter); vesicular nucleus with an

endosome; 50-125/1 long during locomotion; fresh water. A. vespertilio Penard (Fig. 185, b, c.) Pseudo podia conical, comparatively short, connected at base by web-like expansions of ectoplasm; endoplasm colorless, with numerous granules and food particles; a single vesicular nucleus with a large endosome; contractile vacuoles; 60-100/x long; fresh water. Cannibalism (Lapage, 1922); contractile vacuole (Hyman, 1936) morphology and biology (Raabe,
;

1951).

A. gorgonia P. (Fig. 185, d-f). Body globular when inactive with a variable number of radiating "arms," formed on all sides; when with a large endosome; rounded forms 40-50m in diameter; clavate individuals up to 100m; fresh water among vegetation. A. radiosa Ehrenberg (Fig. 185, g). Small, usually inactive; globular or oval in outline; with 3-10 radiating slender pseudo podia which vary in length and degree of rigidity; when pseudo pods are withdrawn, the organism may be similar to A. proieus in general appearance; pseudo pods straight, curved or spirally coiled; size varies, usually about 30m in diameter, up to 120m or more: fresh water. Genus Dinamoeba Leidy. Essentially Amoeba, but the temporary posterior region of body with retractile papillae body surface including pseudopods and papillae, bristling with minute spicules or motionless cils; often surrounded by a thick layer of delicate hyaline jelly, even during locomotion; fresh water. D. mirabilis L. (Fig. 185, h). Oval to limaciform; spheroid when floating; pseudo podia numerous, conical; ectoplasm clear, usually with cils; endoplasm with food vacuoles, oil (?) spherules and large
in locomotion, clavate; nucleus vesicular,
;

clear globules; nucleus and contractile vacuole obscure; spherical forms 64-160m in diameter; creeping forms 152-340/x by 60-220m; cyst about 160m in diameter (Groot, 1936); in sphagnous swamp. Genus Pelomyxa Greeff. Large amoeboid organisms, ranging from

0.5 to 4 or 5

mm.

in length

when

clavate and

moving progressively;

nuclei numerous, less than 100 to 1000 or more;

tile

many small

contrac-

vacuoles; refringent bodies ("Glanzkorper") of various dimen-

sion

and number; with or without bacterial inclusions (which Penard and others consider as symbiotic); holozoic on plant or animal organisms or detritus; plasmotomy simple or multiple; in fresh water. Several species (Kudo, 1946). Nomenclature (Schaeffer, 1926; Mast and Johnson, 1931; Rice, 1945; Kudo, 1946, 1952; Wilber, 1947).

AMOEBINA
P. palustris G. (P. villosa Leidy) (Fig. 186,
undifferentiated cytoplasm with
a).

441

Large; 2-3

mm.

or

larger in diameter; sluggish, with usually one broad

pseudopodium;

many

nuclei

and various inclusions

such as fragments of plant bodies, numerous small sand particles, etc., which brings about opacity and dark coloration of body; in addition bacteria (Cladothrix pelomyxae Veley, Myxococcus pelomyxae Keller and Bacterium parapelomyxae Keller) occur in the cytoplasm

Pelomyxa palustris, X160 (Leidy); b, c, P. carolinensis, an individual in locomotion; c, feeding form); d, e, P. illinoisensis, X40 (Kudo) (d, an individual in locomotion; e, a more or less stationary animal); f, Vahlkampfia patuxent, X660 (Hogue); g, h, Acanthamoeba castellanii, X1270 (Hewitt); i, j, A. hyalina, X840 (DoFig. 186.
a,

X45 (Kudo)

(b,

bell).

which some observers consider as symbionts; cyst with two to three

envelopes (Stole, see Kudo, 1951) feeds on plant and inorganic debris; polysaprobic in still stagnant water, buried in mud. Central
;

Europe, Great Britain and North America. Morphology (Greeff, 1874; Hollande, 1945); locomotion (Okada, 1930a; Mast, 1934); plasmogamy (Okada, 1930) laboratory cultivation (Hollande, 1945).
;

442

PROTOZOOLOGY

P. carolinensis Wilson (Figs. 66; 71; 186, b, c). Monopodal forms 1-5 mm. long; polypodal forms 1-2 mm. in diameter; locomotion ac-

up to 1000 or more, circular in front view, about 20/x in diameter and ellipsoid in profile; fluid and food vacuoles, crystals,
tive; nuclei

on various Protozoa and inverteplasmotomy into two to six individuals; nuclear division simultaneous and synchronous; experimental plasmogamy; no encystment in the Illinois stock, but New Jersey stock is said to encyst (Musacchia, 1950); North America. Distribution (Kudo, 1946); morphology (Wilson, 1900; Andresen, 1942; Kudo, 1946); plasmotomy (Schaeffer, 1938; Kudo, 1949); nuclear division (Kudo, 1947); locomotion (Wilber, 1946); permeacontractile vacuoles; feeds
brates; easily cultivated in laboratory;
bility

many

(Belda,

1942-1943); effect of x-irradiation (Daniels, 1951,

1952, 1952a).

P. illinoisensis Kudo (Fig. 186, d, e). The organism resembles the last-named species, but much smaller in size; 500-1000 // in length;
clavate forms seldom exceed 1.5
cal,

mm.;

several

hundred

nuclei, spheri-

14-16/z in diameter; peripheral granules of the nuclei are large

discoid, irregularly distributed; crystals occur

abundantly chalky white in reflected light; plasmotomy into two to five daughters; encystment and excystment take place freely in cultures; cysts measure 250-350^ in diameter with usually two membranes, a multinucleate amoeba emerges from a cyst after several weeks (Kudo, 1950, 1951). Other species of Pelomyxa (Kudo, 1951). Genus Vahlkampfia Chatton and Lalung-Bonnaire. Small amoein all physiological conditions;

and often

bae; vesicular nucleus with a large endosome and peripheral chro-

matin; with polar caps during nuclear division; snail-like movement, with one broad pseudo podium; cysts with a perforated wall; fresh

water or parasitic. Nuclear division

V.

(Jollos, 1917).

Umax

(Dujardin).

30-40/x long; fresh water.

V. patuxent

Hogue

(Fig. 186, /).

In the alimentary canal of the

first

oyster; about 20^ long during the

few days of

artificial culti-

vation, but later reaching as long as 140/* in diameter; ordinarily

one large broad fan-shaped pseudopodium composed of the ectoplasm; in culture, pseudopodium-formation eruptive; holozoic on
bacteria; multiplication

by

fission or

budding; encystment rare;

cysts uninucleate.

Genus Hartmannella Alexeieff. Small amoebae, with moderately or well-developed ectoplasm; vesicular nucleus with a large endosome; mitotic figure ellipsoidal or cylindrical, without polar caps.
Cysts rounded; wall smooth or slightly wrinkled in one species.

AMOEBINA

443

Several species. Volkonsky (1933) distinguishes four groups. Species

and morphology (Singh, 1952); nuclear division (Jollos, 1917). H. hyalina (Dangeard). 20-25/z in diameter; ectoplasm well developed; endoplasm vacuolated; slender pseudo podia extend in different directions; Hartmann and Chagas observed a centriole in
the endosome.

Genus Acanthamoeba Volkonsky. Small amoebae

mannella; ectoplasm
is

similar to Hart-

not well developed; mitotic figure at the end of metaphase, a straight or concave spindle with sharply pointed poles. Cysts enveloped by two membranes, the outer envelope being
highly wrinkled and mammillated. Several species.

A. castellanii (Douglas) (Fig. 186,

g, h).

In association with fungi

and certain bacteria; Hewitt obtained the organism from agar cultures of sample soil taken from among the roots of white clover; coexisting with yeast-like fungi, Flavobacterium trifolium and Rhizobium sp.; 12-30/x in diameter; some cysts are said to remain viable
at 37C. for 6 days.

A. hyalina (Dobell and O'Connor) (Fig. 186, *, j). According to Volkonsky, the organism described by Dobell and O'Connor as Hartmannella hyalina, is transferred to this genus. Small amoeba; 9-17yu in diameter when rounded; a single contractile vacuole; binary
fission; mitotic figure

10-15/x in diameter; with a

wall; easily cultivated
soil

a sharply pointed spindle. Cysts spherical; smooth inner and a much wrinkled outer

from old faeces of man and animals; also in and fresh water. Genus Sappinia Dangeard. With two closely associated nuclei. S. diploidea (Hartmann and Nagler). Coprozoic in the faeces of different animals; pseudopodia short, broad, and few; highly vacuolated endoplasm with 2 nuclei, food vacuoles, and a contractile vacuole; surface sometimes wrinkled; the nuclei divide simultaneously; during encystment, two individuals come together and secrete
a common cyst wall; 2 nuclei fuse so that each individual possesses a single nucleus; finally cytoplasmic masses unite into one; each nucleus gives off reduction bodies (?) which degenerate; 2 nuclei now come in contact without fusion, thus producing a binucleate
cyst

(Hartmann and Nagler).

Family 3 Endamoebidae Calkins

Exclusively parasitic amoebae; the vegetative form

tractile vacuoles absent, except in

is

relatively

small and occurs mostly in the alimentary canal of the hosts; con-

Hydramoeba;

multiplication

by
is

binary

fission;

encystment common. The generic differentiation

444

PROTOZOOLOGY

based upon the morphological characteristics of the nucleus. Summary No. 99 of 'Opinions Rendered' by the International Commission of Zoological Nomenclature (1928) holds that Entamoeba is a synonym of Endamoeba; in the present work, however, Endamoeba and Entamoeba are separated, since the two groups of species placed under them possess different nuclear characteristics (Fig. 187). Nomenclature (Dobell, 1919, 1938; Kirby, 1945; Hemming, 1951). Genus Endamoeba Leidy (1879). Nucleus spheroidal to ovoid; membrane thick; in life, filled with numerous granules of uniform dimensions along its peripheral region; upon fixation, a fine chromatic network becomes noticeable in their stead; central portion

Diagram showing the stained nuclei of the trophozoites of five genera of parasitic amoebae, a, Endamoeba; b, Entamoeba; c, Iodamoeba; d, Endolimax; e, Dientamoeba.
Fig. 187.

with several endosomes between the two zones cytoplasm becomes prominently striated during locomotion; in the intestine of invertebrates. E. blattae (Biitschli) (Fig. 188). In the colon of cockroaches; 10coarsely reticulated
(Fig. 187, a)
; ;

in some,

150 n in diameter; rounded individuals with broad pseudopodia, show a distinct differentiation of cytoplasm; elongated forms with a few

pseudopodia, show ectoplasm only at the extremities of the pseudopods; endoplasm of actively motile trophozoites shows a distinct
striation, a condition

not seen in other amoebae;

fluid-filled

vacuoles
cells,

occur in large numbers; amoebae feed on starch grains, yeast

and

bacteria, all of

which coexist

in the host organ; cysts,

20-50m

in diameter,

commonly

seen in the colon contents, with often more

is still

than 60 nuclei. The

life-cycle of this

rier (1909) held that

amoeba when the multinucleate

its

unknown. Merbecomes

cysts gain entrance to

the host intestine through the center of a gamete;

mouth, each

of the cyst-nuclei

when the cyst-membrane

ruptures, the

gametes are

set free

and anisogamy takes

place, resulting in forma-

AMOEBINA
tion of
zoites.

445

numerous Morphology (Leidy, 1879; Kudo, 1926; Morris, 1936; Meg-

zygotes which develop into the habitual tropho-

litsch, 1940).

E. thomsoni Lucas. In the colon of cockroaches; 7-30/x in diameter; very adhesive; 1-3 large peripheral granules on the nuclear membrane; cysts 8-16ju in diameter, with 1-4 nuclei (Lucas, 1927).

E. disparata Kirby. In colon of Microtermes hispaniolae ; 20-40^

long; active; xylophagous (Kirby, 1927).

Fig. 188. Endamoeba blattae. a-c, trophozoites in life, X530; d, a stained binucleate amoeba; e, f, stained and fresh cysts, X700 (Kudo).

E. majestas K. (Fig. 189,

a).

diameter;

many

short pseudo podia; cytoplasm

In the same habitat; 65-165ju in rilled with food

In the gut of Microtermes pana-

particles (Kirby, 1927).

E. simulans K. (Fig. 189, maensis; 50-1 50/z in diameter.

b).

E. sabulosa K. In the same habitat; small 19-35/z in diameter.

E. pellucida, E. granosa, E. lutea and E. suggrandis were described

from the colon of Cubitermes

sp. of Africa

(Henderson, 1941).

446

PROTOZOOLOGY

(1895). Nucleus endosome, located in or near the center and with varying number of peripheral nonchromatinic granules attached to the nuclear membrane (Fig. 187, b) chromatin in the endosome and in peri-endosomal region. The genus was established by the two Italian authors who were unaware of the existence of the genus Endamoeba (p. 444). Numerous species in vertebrates and invertebrates; one species in Protozoa.
vesicular, with a comparatively small
;

Genus Entamoeba Casagrandi and Barbagallo

Fig. 189. (Kirby);

a,
c,

Endamoeba majestus, X420 (Kirby); b, E. simulans, X420 Entamoeba paulista in Zelleriella, X290 (Stabler and Chen).

E. histolytica Schaudinn (1903) (Figs. 190, 191).

is

The trophozoite

an active amoeba and measures 7-35 (9-20) n in diameter; cytoplasm usually well differentiated; eruptive formation of large lobopodia, composed largely of ectoplasm; when fresh, active monopodal
progressive

movement; the

vesicular nucleus appears in

life

as a

ring, difficult to recognize;

cell

food vacuoles contain erythrocytes, tissue

fragments, leucocytes, etc.; stained nucleus shows a membrane,

comparatively small peripheral granules, a centrally located small endosome and an indistinct network with a few scattered chromatin granules. The trophozoite multiplies by binary fission. The amoeba
lives in the

lumen and

in the tissues of the wall of the colon,

is

and

brings about characteristic ulceration of the colon which

typically

accompanied by symptoms
vein, the

of amoebic dysentery.
liver in

Through the portal

it

amoeba may invade the

is

which

produces abscess,

and other organs such as lung,

these organs

brain, testis, etc.

The

infection in

referred to as amoebiasis.

Under certain circumstances not well understood, the amoebae remain small after division. Such amoebae are sluggish and known

AMOEBINA
as the precystic forms.

447

amoeba secretes presently a resistant wall and becomes encysted. The highly refractile cyst is spherical and measures 5-20/* in diameter. At first it contains a single nucleus which divides twice. The mature cyst contains four nuclei.
precystic

The

In addition the cyst contains diffused glycogen and elongated refracrod-like bodies with rounded extremities which stain deeply with haematoxylin (hence called chromatid bodies). These inclusions are absorbed and disappear as the cyst matures. No further changes
tile

up
Pi ''KJ_

we
.

-V

:;

,W,

IPS Q
7

Fig. 190. Entamoeba histolytica, 2-4, stained trophozoites;

X1150 (Kudo).
5,

a living trophozoite; a fresh cyst; 6-9, stained cysts.

1,

take place in the cyst as long as it remains outside the host's intestine. The trophozoites are found in dysenteric or diarrhoeic faeces,

but formed faeces usually contain cysts. The cyst is the stage by which the organism begins its life in a new host. The life-cycle of Entamoeba histolytica in human host is unknown. The amoeba has, however, been cultivated in vitro by numerous investigators since the first successful cultivation by Boeck and Drbohlav (1924) (p. 887). The excystment of cysts and metacystic development have also been observed and studied especially by Dobell (1928) and Cleveland and Sanders (1930) in cultures. Snyder

448

PROTOZOOLOGY

and Meleney (1941) found that bacteria-free cysts usually excyst when suspended in various media with living bacteria and in the absence of bacteria, excystment was observed only in the presence
of the reducing agents, cysteine or neutralized thioglycollic acid or

under conditions of reduced oxygen tension. According to Dobell, in the process of excystation, a single tetranucleate amoeba emerges from a cyst through a minute pore in the cyst wall. The tetranucleate metacystic amoeba produces a new generation of trophozoites by a diverse series of nuclear and cytoplasmic divisions (Fig. 191) which result in production of eight uninucleate amoebulae. These amoebulae are young trophozoites which grow into larger ones. No sexual phenomena have been observed during these changes. It is supposed
that

when

viable cysts reach the lower portion of the small intestine

or the colon, the changes stated above take place in the

lumen and

the young uninucleate amoebulae initiate an infection.

Q)
I
I

G
I

cbeb / 0[
I
\

Fig. 191. Diagram showing excystment and a common way by which a metacystic amoeba of Entamoeba histolytica divides into 8 uninucleate

amoebulae (Dobell).

AMOEBINA
While the description
of

449

Entamoeba

histolytica given

above applies

dimensions of trophozoites and cysts, and in pathogenicity in human host as well as in experimental animals
in general, diversities in

have been reported.

A number

of observers are inclined to think

that there are several varieties or races of this amoeba,

as

has

already been mentioned

(p. 226).

Entamoeba amoeba," was

It is

histolytica,

first definitely

commonly known as "the dysentery recognized by Losch in Russia in 1875.

although
it is

now known
The

to be widely distributed in tropical, subtropical

alike,

and temperate regions

regions.

more prevalent

in

warmer

incidence of infection depends mainly on the sanitary

conditions of the community, since the cysts of the organism are

voided from host in faeces. Faecal examinations which have been

carried on

by numerous

investigators in different countries of the

is

world, reveal that the incidence of infection

as high as over 50 per

cent in some areas. According to Craig (1934), 49,336 examinations made by many observers in various parts of the United States show

that the infection rate varied from 0.2 to 53 per cent, averaging 11.6
per cent, which justifies Craig's (1926) earlier estimate that about 10 per cent of the general population harbor this protozoan.
infection

An

acute
in

by E.

histolytica

is

accompanied by dysentery, while

chronic cases or in convalescence, the host

as a cyst-carrier or -passer.

may

void infectious cysts

is

without suffering from the infection himself. Such a person

known

The trophozoite if voided in faeces perish in a comparatively short The dissemination of infection is thus exclusively carried on by the cyst. Viable cysts may be transmitted (1) by contamination of
time.

food through contact with contaminated water or through unsani-

who are cyst-carriers; (2) by droppings of and cockroaches which, as noted below, contain viable cysts for a comparatively long time after feeding on faeces containing cysts and by soiled appendages of these insects which may directly transfer the cysts to food by walking on it; and (3) by contaminated water in which the cysts live considerably longer than in faeces (p. 450). The seriousness of water-borne infection in crowded areas is easily realized when one recalls the outbreak (some 1400 cases) of amoebic dysentery and amoebiasis which originated in Chicago in 1933, where defective plumbing in certain establishments contaminated the water system with the cysts of Entamoeba histolytica (Bundesen et al., 1936) and the development of some 100 cases of amoebic dysentery among firemen who drank contaminated water in connection with the 1934 fire of the Union Stockyards in Chicago (Hardy and Spectary habit of food handlers
flies

tor),

although

in

the latter instance, some workers believe that se-

450

PROTOZOOLOGY
may have
infections aided

vere amoebic infections

dormant
teria.

resulted from already existing by the newly formed association with bac-

the

The cysts remain viable for a considerable length of time outside human intestine, if environmental conditions are favorable. Since

information regarding the viability and longevity of the cyst is highly important from the epidemiological standpoint, many papers

have dealt with it. In testing the viability of the cyst, the following two tests have been used by the majority of investigators. (a) Eosin-staining test. Kuenen and Swellengrebel (1913) first used a dilute solution of eosin (1:1000). It has since been used by Wenyon and O'Connor, Root, Boeck, and many others. Solutions used vary from 1:10,000 (Root) to 1:100 (Boeck). A small amount of fresh cyst-containing material and a drop of eosin solution are mixed on a slide, then dead cysts will appear stained reddish under the microscope, while living cysts remain unstained. Whether or not unstained cysts might be dead or uninfectious is unknown. But as Wenyon and O'Connor wrote, "if we accept the eosin test as a criterion and regard all unstained cysts as living, the error in judgment will be on the safe side." Root found neutral red in 1:10,000
dilution to give a slightly larger proportion of stained cysts than
eosin.

Frye and Meleney's (1936) comparative study leads one

to

look upon this method as a fairly dependable one.

(b) Cultivation test. Improved cultural technique now brings about easily excystment of viable cysts in a proper culture medium. For example, Yorke and Adams (1926) obtained in 24 hours "a plentiful growth of vegetative forms" from cysts in Locke-egg-serum medium (p. 887). Snyder and Meleney (1941) note recently that the excystation does not take place in various culture media unless living bacteria were added or oxygen concentration of the media was decreased. Animal infection method has not been used much, as experimental animals (cats) show individual difference in susceptibility.

testing

tion
1.

of the published results are summarized below. The method used is indicated by: a for eosin test or 6 for cultivatest and is given after the name of the investigators.

Some

Cysts in faeces kept in a covered container. All cysts disap-

peared in 3 days at 37C; at 27-30C. half of the cysts found dead by the 4th and all dead by the 9th day (Kuenen and Swellengrebel
Alive for 3 weeks (Thomson and Thomson; a). Remain unchanged for several weeks if kept "cool and moist" (Dobell). All dead within 10 days at 16-20 or 0C. (Yorke and Adams; b). 2. Cysts kept in water emulsion. All alive on the 9th, but almost
a).

AMOEBINA
all
;

451

dead on the 13th day (Kuenen and Swellengrebel a). Viable for 25 days (Thomson and Thomson; a). Cysts in running water for 15 days, excysted in pancreatic juice (Penfold, Woodcock and Drew). Viable for 30 days (Wenyon and O'Connor; a) for 5 weeks (Dobell) for 153 days (Boeck; a). Alive for 10 and 17 days at 16-20 and 0C.
;

respectively (Yorke
30, 20, 10
3.

and Adams; 6); for 3, 10, 30, and 90 days and 0C. respectively (Chang and Fair; b).

at

Cysts in relation to high temperatures. Cysts are killed at

68C. in 5 minutes (Boeck; a); at 50C. in 5 minutes (Yorke and Adams; 6). Dipping in boiling water for 5-10 seconds kills the cysts
(Kessel; a).
4.

Cysts in relation to desiccation. Desiccation

kills

cysts instantly

(Kuenen and Swellengrebel; Wenyon and O'Connor, Dobell, etc.). Therefore, the cysts carried in dust are most probably not viable
under ordinary circumstances. 5. Cysts in relation to chemicals.

HgCl 2 0.1%
.

solution kills cysts in 4 hours

;

(Kuenen and
kills

Swellengrebel; a)
Creolin.

kills

readily (Lin;

6).

2500 solution

cysts in 30 minutes at 20-25C. (Yorke

1

:250 solution

kills

cysts in

and Adams; 6). 5-10 minutes (Kuenen and

Swellengrebel; a).
Alcohol.

50%

alcohol kills cysts immediately

(Kuenen and

Swellengrebel; a); in one hour (Kessel; a).

Formaldehyde. Cysts treated in 1% solution for 4 hours were apparently dead, though not stained with eosin (Wenyon and O'Connor). 0.5% solution kills cysts in 30 minutes at 20-25 or 37C. (Yorke and Adams; b). Cresol. 1:20, 1:30, and 1:100, killed the cysts immediately, in one minute and in 30 minutes respectively (Wenyon and O'Connor; a). Phenol. 1:40 and 1:100 killed cysts in 15 minutes and 7 hours respectively (Wenyon and O'Connor; a). 1% solution of phenol or lysol kills cysts in 30 minutes at 20-25 or 37C.
(Yorke and Adams; b). HC1. 7.5% solution at 20-25C. and 5% at 37C. kill the cysts in 30 minutes (Yorke and Adams; 6). NaOH. 2.5% solution kills cysts in 30 minutes at 20-25 or 37C. (Yorke and Adams; 6). Chlorine. 1:10,000 solution did not have any effect on cysts after several hours (Wenyon and O'Connor; a). 0.2% and 0.5% solutions kill the cysts in 7 days and 72 hours respectively (Kessel; a). 0.5% and 1% solutions kill the cysts in

452

PROTOZOOLOGY
36-48 and 12-24 hours respectively (Lin;
1/64 of a 6). saturated solution of chlorine (about 0.7 weight %) at

20-25C. and 1/320 solution at 37C. killed the cysts in 30 minutes (Yorke and Adams; b). Exposure to the residual chlorine 5, 8 and even 10 parts per million for 30 minutes allowed cysts to remain viable (Becker et al.). Thus the cysts
of E. histolytica are resistant to chlorinated

the concentration which

is

water far above used ordinarily in water treatkills

ment. Potassium permanganate.

(Kessel; a).
1

2% solution
kills
kill

the cysts in 3 days

b).

:500 solution

cysts in 24-48 hours (Lin;

]%

solution does not

cysts at 20-25 or 37C. in 30

minutes (Yorke and Adams; b). Emetin hydrochloride and yatren. 5% solutions of the two drugs did not have any effects upon cysts at 20-25 or 37C. in 30 minutes (Yorke and Adams; 6).
Antibiotics.
of antibiotics appear to inhibit the which results in the death of the amoeba in culture. Prodigiosin, however, according to Balamuth and Brent (1950), kills the amoebae when added in the dilution

The majority

growth

of bacteria,

of 1:400,000, while bacterial flora, oxidation-reduction po-

tentials

and

pH

are not affected

by

it.

Cysts in relation to passage through the intestine of insects. that the cysts of E. histolytica survived as long as 24 hours in the intestines of flies, Musca domestica, Calliphora, and Lucilia, and living cysts were voided for 16 hours after feeding on faecal material containing cysts. Roubaud using Musca domestica, found also unaltered cysts for over 24 hours (but rarely after 40 hours) after taking the cysts in its gut, and if a fly drowned in water, the cysts remained viable for about a week. Root (1921) using Musca domestica, Calliphora erythrocephala (and Fannia caniadaris, Lucilia caesar, and Chrysomyia macellaria) found that about half the cysts were dead after 15 hours and last living cysts were found after 49 hours in the intestines of these flies after feeding on cyst-containing material, and that when the flies which ingested cysts were drowned in water, about half the cysts were found dead in 3 days and last living cysts were noticed on the 7th day. Frye and Meleney (1932) found cysts in the intestines of flies which were caught in 4 of 12 houses where infected subjects lived. Macfie (1922) reported that the cysts of Entamoeba histolytica he observed in the intestine of Periplaneta americana appeared un6.

Wenyon and O'Connor found

AMOEBINA

453

harmed. Tejera (1926) reports successful experimental infection in two kittens that were fed on the droppings of cockroaches (sp.?) caught in a kitchen, which contained cysts resembling those of E. histolytica. Frye and Meleney (1936) observed that the cysts passed through the intestine of Periplaneta americana in as early as 10-12 hours and remained in the intestine for as long as 72 hours, after feeding on experimental material. Cysts which stayed in the cockroach intestine for 48 hours gave good cultures of trophozoites
in

egg-horse-serum-Ringer medium.

'0

S
Fig. 192. Entamoeba

6
coli,

X1150 (Kudo). 1, a living amoeba; 2-5, stained trophozoites; 3, an amoeba infected by Sphaerita; 6, a precystic amoeba; 7, a fresh cyst; 8, a stained young cyst with a large glycogen
vacuole;
9,

a stained mature cyst.

histolytica, there are

In addition to E.
intestinal

now known
coli,

four other

Endolimax nana, Iodamoeba biitschlii and Dientamoeba fragilis. In Table 10 are given the characteristics necessary for distinguishing E. histolytica from the other four intestinal amoebae. E. coli (Grassi) (Fig. 192). The trophozoite measures 15^0/* in diameter; average individuals 20-35/x; cytoplasm not well differentiated; movement sluggish; endoplasm granulated, contains microorganisms and faecal debris of various sizes in food vacuoles; erythrocytes are not ingested, though in a few cases (Tyzzer and Geiman)
living in

amoebae

man. They are E.

454

PROTOZOOLOGY

if

AMOEBINA
and
in culture (Dobell, etc.),

455

they
is

(see below); nucleus, 5-8ju in diameter, seen in vivo;

E. histolytica, the endosome

ter)

be taken in as food particles compared with somewhat large (about 1m in diame-

may

and located

eccentrically; peripheral granules

more conspicuous.
is

The

precystic form, 10-30/x in diameter, resembles that of E. his-

tolytica.

Separation of the two species of amoebae by this stage

is

ordinarily impossible.

The

cyst

spherical or often ovoid, highly refractile; 10-30^ in

1,

diameter; immature cyst contains

2 or 4 nuclei, oneor more large

glycogen bodies with distinct outlines, but comparatively small number of acicular, filamentous or irregular chromato id bodies with sharply pointed extremities; when mature the cyst contains 8 nuclei and a few or no chromato id bodies. The trophozoites and
small

number

of cysts occur in diarrhoeic or semiformed faeces

and

the formed faeces contain mostly cysts.

lumen of the colon and does not enter the As noted above, it has been observed in a few instances to ingest erythrocytes, but there is no evidence to show that it takes them in from living tissues. This amoeba is therefore considered a commensal. The abundant occurrence of the trophozoite in diarrhoeic faeces is to be looked upon as a result and not
This amoeba
lives in the

tissues of the wall.

the cause of the intestinal disturbance. This amoeba is of common occurrence and widely distributed throughout the world. Nothing is known about its life-cycle in the human intestine.

Cultivation of cysts in vitro indicates, according to Dobell (1938), the following changes The cyst content usually emerges as a single
:

multinucleate

amoeba through a

large opening in the cyst wall.

Prior to or during the emergence, the

amoeba may

divide.

Normal

mature cysts "frequently lose" 1-4 of their original 8 nuclei before germination, thus becoming "infranucleate" (with 4-7 nuclei). Unlike in E. histolytica, there is

no nuclear division
finally

in the

metacystic
distribu-

stages.

By

a series of binary divisions with

random nuclear

tion, uninucleate

amoebulae are

produced. These are young

amoebae which develop into large trophozoites. Here also, there is no sexual phenomenon in the life-cycle. Nomenclature and morphology (Dobell, 1919, 1938). E. gingivalis (Gros) (E. buccalis Prowazek) (Fig. 193). This amoeba lives in carious teeth, in tartar and debris accumulated around the roots of teeth, and in abscesses of gums, tonsils, etc. The trophozoite is as active as that of E. histolytica; 8-30> (average 10-20>) in diameter; cytoplasm well differentiated; monopodal progressive movement in some individuals; endoplasm hyaline, but

456

PROTOZOOLOGY
number
of pale greenish
cells

vacuolated, and contains ordinarily a large

bodies (which are probably nuclei of leucocytes, pus

or other

degenerating host
in diameter,

cells)

and bacteria
;

in food vacuoles; nucleus, 2-4/x

it

appears as a ring when stained

shows a small central

endosome and small peripheral granules

closely attached to the

Si
~Qm m
-V-. A

<#**

Fig. 193. Entamoeba gingivalis, X1150 (Kudo). 3-7 stained amoebae.

1, 2,

living

amoebae;

membrane. Stabler (1940) observed 5 chromosomes during binary fission. Encysted forms have not been observed in this amoeba. Kofoid and Johnstone (1930) reported having seen the same organism in the mouth of monkeys (Rhesus and Cynomolgus) from southeast Asia.

E. gingivalis

is

the very

first

parasitic
it

amoeba that has become

known

Russia in the tartar on the surface of the teeth. Some observers maintain that this amoeba is the cause of pyorrhoea alveolaris, but evidence for such an assumption seems to be still lacking. It has been found in the healthy gums and even in false teeth (Lynch). Therefore, it is generally considered as
to

man. Gros (1849) found

in

is widely distributed and of common occurrence. In the absence of the encysted stage, it is supposed that the organism is transmitted in trophic forms. According to Koch (1927) who studied the effects of desiccation and temperatures upon the

a commensal. It

amoeba

in culture, the

amoeba

is

killed at 0C. in 18 hours, at 5C.

48 hours, at 45C. in 20 minutes, at 50C. in 15 minutes, and at 55C. in 2 minutes. At 40C, the survival is said to be for an indefinite length of time. Complete desiccation of the culture medium or immersion in water at 60C. kills the amoeba. She
in 24 hours, at 10C. in

AMOEBINA
considered that E. gingivalis
(Stabler, 1940; Noble, 1947).

457

may

be disseminated both by direct

contact and by intermediate contaminated articles. Nuclear division

E. gedoelsli Hsiung (E. intestinalis (Gedoelst)). In the colon and of horse; 6-13ju by 6-1 1/x; endosome eccentric; bacteriaE. equi Fantham. 40-50m by 23-29^; nucleus oval; cysts tetranucleate, 15-24/z in diameter; seen in the faeces of horse;

caecum
feeder.

Fantham

reports that the endoplasm contained erythrocytes.

E. bovis Liebetanz. 5-20/x in diameter; uninucleate cysts, 4-15/z in diameter; in the stomach of cattle and gnu, Cunnochaetes taurinus

(Mackinnon and Dibb, 1938). Morphology (Noble, 1950). E. ovis Swellengrebel. Cyst uninucleate; in the intestine E. caprae Fantham. In goat intestine.
cyst uninucleate, 5-1 1/z in diameter.

of sheep.

E. polecki (Prowazek). In the colon of pigs; 10-12/z in diameter; E. debliecki Nieschulz (Fig. 194,
nucleate; in the intestine of pigs
;

a). 5-lO^t in

diameter; cysts uni-

and goats. Two races (Hoare, 1940) morphology (Nieschulz, 1924) Entamoebae of domestic animals (Noble and Noble, 1952).
E. venaticum Darling. In the colon of dog; similar to E. histolytica;
since the

dog

is

experimentally infected with the latter, this

liver, is

amoeba

discovered from spontaneous amoebic dysentery cases of dogs, in

one of which were noted abscesses of

stages; in the intestine of rabbits.

probably E.

histolytica.

E. cuniculi Brug. Similar to E. coli in both trophic and encysted

E. cobayae Walker (E. caviae Chatton). Similar to E. coli;

intestine of guinea-pigs (Nie, 1950).

in

the

E. muris (Grassi) (Fig. 194,

b, c).

In the caecum of rats and mice;

trophozoite 8-30 /z; cytoplasm with rod-shaped or fusiform bacteria

and
ter

flagellates coinhabiting the host's organ; nucleus 3-9/* in

diame-

and resembles

closely that of E. coli; cysts 9-20/x in diameter,

with eight nuclei when mature. Nuclear division (Wenrich, 1940);

food habits (Wenrich, 1941).
E.
citelli

Becker (Fig. 194,

in

d, e).

In the caecum and colon of the

striped ground squirrel, CiteUus tridecemlineatus ; rounded trophozoites

10-25m

diameter; nucleus 4-6/* in diameter, with a comparavaries in position

tively large

endosome which

from central to

perpheral; cysts with eight nuclei, about 15m in diameter. E. gallinarum Tyzzer. In the caeca of chicken, turkeys and possibly other fowls; trophozoites

9-25 (16-18)//; cysts octonucleate,

15^ bv

12ju.

458

PROTOZOOLOGY

E. testudinis Hartmann. In intestine of turtles, Tesludo graeca, T. argentina, T. calcarata and Terrapene Carolina.

snapping

E. barreti (Taliaferro and Holmes) (Fig. 194, /). In the colon of turtle, Chelydra serpentina; trophozoites 14-23 (18)^ long.
g, h).

Cultivation (Barret and Smith, 1924).

E. terrapinae Sanders and Cleveland (Fig. 194,

Trophozoites

10-15/x long; cysts 8-14/z in diameter, tetranucleate

when mature;

a, a stained cyst of Entamoeba debliecki, X1330 (Hoare); E. muris, X1330 (Wenrich) (b, with fusiform bacilli; c, with Tritrichomonas muris); d, e, stained trophozoite and cyst of E. citelli, X880 (Becker); f, a stained trophozoite of E. barreti, X1330 (Taliaferro and Holmes); g, h, stained trophozoite and cyst of E. terrapinae, X1665 (Sanders and Cleveland); i, j, stained trophozoite and cyst of E. invadens,

Fig. 194.

b, c,

X1045 (Geiman and

Ratcliffe).

upon excystment, the cyst content divides into four uninucleate amoebulae; in the colon of Chrysemys elegans (Sanders and Cleveland, 1930).

E. invadens Rodhain (Figs.

tica.

2, a, b; 194, i,j).

Resembles E.

histoly-

Trophozoites measure 15.9/x in average diameter (9. 2-38. 6 /z by 9-30m); active locomotion; feed on leucocytes, liver cells, epithelial cell debris, bacteria, etc.; nucleus simliar to that of E. histolytica. Cysts 13. 9m (11-20/z) in diameter; 1-4 nuclei; glycogen vacuole;

chromatoid bodies acicular, rod-like or cylindrical. Hosts include various reptiles: Varanus salvator, V. varius, Tiliqua scincoides, Pseudoboa clelia, Lampropeltis getulus, Ancis-

AMOEBINA

459

trodon mokasen, Natrix rhombifer, N. sipedon, N. sipedon sipedon,

N. cyclopion, Python sebae, Rachidelus brazili, etc. Zoological Gardens in Philadelphia (Geiman and Ratcliffe) and Antwerp (Rodhain). The amoeba produces lesions in the stomach, duodenum, ileum, colon and liver in host animals. Time for excystation in host's intestime for metacystic develseven-24 hours; the excysted amoeba with four nuclei, each of which divides once, divides finally into eight amoebulae; optimum temperature for culture 20-30C. (Geiman and Ratcliffe, 1936). Ratcliffe and Geiman (1938) observed spontaneous and experimental amoebiasis in 32 reptiles. E. ranarum (Grassi). In colon of various species of frogs; resembles E. histolytica; 10-50/x in diameter; cysts are usually tetranucleate, but some contain as many as 16 nuclei; amoebic abscess of the liver was reported in one frog. Comparison with E. histolytica
five to 14 hours;

tine (jejunum

and ileum)

opment

in host's intestine

(Dobell, 1918);

life

cycle (Sanders, 1931).

E.
ian,

Mackinnon and Ray. In the intestine of the ascidPhallusia mamillata; 15-30m by 10-15m; nucleus about 5ju in
(?)

phallusiae

diameter, structure not well defined; cysts uninucleate, about 20/z

in diameter; parasitic nutrition.

E. minchini Mackinnon. In gut of tipulid larvae; 5-30/x in diameter; cyst nuclei

up

to 10 in

number.

E. apis

Fantham and

Porter. In

Apis

mellifica; similar to E. coli.

when rounded 7-30 (15-25)m in diameter; usually attached to debris by a knoblike process, highly adhesive; cytoplasm poorly differentiated; vesicular nucleus with peripheral granules; endosome variable, with loosely aggregated granules and a central dot; cysts 8-16/x in diameter, with one to four nuclei (Lucas, 1927). E. aulastomi Noller. In the gut of the horse-leech, Haemopis sanguisuga; cysts with four nuclei. Morphology nad development
E. thomsoni Lucas. In the colon of cockroaches;
(Bishop, 1932).

E. paulista (Carini) (Brumptina paulista C.) (Fig. 189,

c).

In the

cytoplasm of
in

many

species of Protociliata; trophozoites 5.3-14. 3/z

9.4/x in

diameter; cysts about

diameter, uninucleate; no effect upon

host ciliates even in case of heavy infection (Stabler and Chen, 1936;

Chen and
8-14jii in

Stabler, 1936). Carini

and Reichenow (1935) trophozoites

:

diameter; cysts 8-12/i; either identical with E. ranarum or

it.

a race derived from

Genus Iodamoeba Dobell. Vesicular nucleus, with a large endosome rich in chromatin, a layer of globules which surrounds the endosome and do not stain deeply, and achromatic strands between

400 the endosome and

PROTOZOOLOGY
membrane
(Fig. 187, c); cysts ordinarily uninuglycogenous vacuole which stains conspicu-

cleate, contain a large

ously with iodine; in intestine of

I. butschlii

zoite

is

man and mammals (Dobell, 1919). (Prowazek) (7. williamsi P.) (Fig. 195). The tropho6-25/x (average 8-1 5/z) in diameter; fairly active with pro-

gressive

movement, when fresh; cytoplasm not well differentiated; endoplasm granulated, contains bacteria and yeasts in food vacuendo\ the diameter of nucleus, surrounded

oles; the nucleus (3-4/x in diameter) visible in vivo; the large

some about

by small spherules.

.;.

'

Fig. 195. Iodamoeba butschlii, X1150 (Kudo). 1, a living amoeba; 2-5, stained trophozoites; 4, 5, somewhat degenerating trophozoites; 0, a fresh
cyst; 7-10, stained cysts.

The cysts are spherical, ovoid, ellipsoid, triangular, pyriform or square; rounded cysts measure about 6-1 5/* in the largest diameter; a large glycogen body which becomes conspicuously stained with
Lugol's solution (hence formerly called "iodine cysts") persists; nucleus with a large, usually eccentric endosome.

The

trophozoites and cysts are ordinarily present in diarrhoeic

faeces, while the

formed faeces contain cysts only. This amoeba apparently lives in the lumen of the colon and does not seem to attack

and is, therefore, considered to be a commensal. Nomenclature (Dobell, 1919); nuclear structure (Wenrich, 1937a). I. suis O'Connor. In colon of pig; widely distributed; indishost's tissues

tinguishable from

I. butschlii; it is

considered

by some that

pigs are

probably reservoir host of

I. butschlii.

Genus Endolimax Kuenen and Swellengrebel. Small; vesicular nucleus with a comparatively large irregularly shaped endosome,

AMOEBINA

461

composed of chromatin granules embedded in an achromatic ground mass and several achromatic threads connecting the endosome with membrane (Fig. 187, d); commensal in hindgut in man and animals.
Several species.
E. nana (Wenyon and O'Connor) (Fig. 196, a-d). The trophozoite measures 6-18ju in diameter; fairly active monopodal movement by forming a broad pseudopodium; when stationary pseudo podia are formed at different points; endoplasm is granulated and contains
bacteria as food particles; the vesicular nucleus, 1.5-3/x in diameter,

composed of a delicate membrane with a few chromatin granules and a large irregularly shaped endosome.
is

Fig. 196. a-d, Endolimax nana, X2300 (Kudo) (a, b, living and stained trophozoites; c, d, fresh and stained cysts); e, f, stained trophozoite and cyst of E. clevelandi, X3000 (Gutierrez-Ballesteros and Wenrich); g, h, stained trophozoites of Martinezia baezi, XI 700 (Hegner and Hewitt).

The cyst is usually ovoid; young cyst

contains

or 2 nuclei; mature

cyst with 4 nuclei; indistinctly outlined glycogen

body may be present while immature; dimensions 5-12/x (majority 7-10/i) in

diameter.

The
is

trophozoites are found in diarrhoeic or semifluid faeces to-

gether with the cysts, and formed faeces contain cysts. This
coelozoic in the

amoeba

upper portion of colon and is considered to be a commensal. Cytology and life-history (Dobell, 1943). E. caviae Hegner. In the caecum of guinea-pigs. Morphology (Heg-

lumen

of the

ner, 1926; Nie, 1950).

462

PROTOZOOLOGY

E. grcgariniformis (Tyzzer). In the caeca of fowls; 4-12ju in diameter; cysts uninucleate (Tyzzer, 1920). E. clevelandi Gutierrez-Ballesteros and Wenrich (Fig. 196, e, /).

In the rectal contents of Pseudemys floridana mobilensis ; trophozoites 5-1 -ijj, in diameter; cysts tetranucleate, 4.5-10/z large.
E. ranarum Epstein and Ilovaisky. In the colon of frogs; cysts
octonucleate,

up to
l^t

25/x in diameter.

E. blattae Lucas. In the colon of cockroaches; trophozoites 3-1 5/z

long; cysts, 7-1
1927).
in

diameter and with one to three nuclei (Lucas,

of

Genus Dientamoeba Jepps and Dobell. Small amoeba; number

forms; nuclear

binucleate trophozoites often greater than that of uninucleate

membrane

delicate;

endosome

consists of several

chromatin granules embedded in plasmosomic substances and connected with the membrane by delicate strands (Fig. 187, e) in
;

colon of

man

(Jepps and Dobell, 1918).

Fig. 197. Dientamoeba fragilis, X2300 (Kudo), a, b, living bi- and uni-nucleate trophozoites; c, d, stianed uni- and bi-nucleate trophozoites.

D. fragilis

J.

and D.

(Fig. 197).

The trophozoite

is

actively

boid; 4-18/x (average 5-12/x) in diameter; progressive

teria in food vacuoles; nucleus onl}r faintly visible;
ratio
is

amoemovement;

cytoplasm well differentiated; endoplasm granulated contains bac1

or 2 nuclei, the

variable; in

some material binucleate forms may be

in others uninucleate

80%

or

more (Jepps and Dobell), while

forms

may pre-

dominate (Kudo, 1926a; Wenrich, 1937); nucleus is made up of a delicate membrane and a large endosome (more than one-half the diameter of nucleus) in which are embedded 4-8 chromatin granules along the periphery. According to Dobell (1940), the binucleate condition represents an arrested telophase stage of mitosis and the chromatin granules are in reality chromosomes, probably 6 in number. Comparison with Histomonas meleagridis (p. 335) led this author to think that this amoeba may be an aberrant flagellate closely related to Histomonas.

AMOEBINA

463

Encysted stage has not been observed. Degenerating trophozoites often develop vacuoles which coalesce into a large one and the organisms may then resemble Blastocystis hominis (p. 893) which is very common in faeces. Transmission may be carried on by trophozoites. According ot Wenrich (1940), this amoeba if left in the faeces remains alive up to 48 hours at room temperature, but disappears probably by disintegration in 2 hours at 3.5C. Since all attempts to bring about experimental infection by mouth or by rectum failed, Dobell considered that the amoeba may be transmitted from host to host in the eggs of nematodes such as Trichuris or Ascaris, as in the case of Histomonas (p. 335). The amoeba inhabits the lumen of the colon. There is no indication that it is histozoic or cytozoic. Some workers attribute certain intestinal disturbances to this amoeba, but no definite evidence for its pathogenicity is available at present. It seems to be widely distributed, but not as common as the other intestinal amoebae mentioned above, although in some areas it appears to be common. Nuclear division (Wenrich, 1936, 1939, 1944a; Dobell, 1940).

Genus Martinezia Hegner and Hewitt. The nucleus

consists of a

wrinkled membrane, a large compact or granular endosome and

heavy peripheral beads; cysts unknown; parasitic. M. baezi H. and H. (Fig. 196, g, h). In the intestine of iguanas, Ctenosaura acanthura; 8-21/* by 6.5-16/*; nucleus about 4/* in diameter; two nuclei in about 3 per cent of the organisms; cysts not seen. Genus Dobellina Bishop and Tate. Trophozoite: small amoeba; ectoplasm and endoplasm differentiated; usually monopodal; nucleus one to many nucleus with a large central endosome and an achromatic nuclear membrane; nuclear divisions mitotic and simul;

taneous; no solid food vacuoles; no contractile vacuole; with refrin-

gent granules. Cysts: spherical; thin-walled; devoid of glycogen and

of

chromatoid bodies; 2 or more nuclei; parasitic (Bishop and Tate,

D. mesnili (Keilin)
(Fig. 198, a-c).

1939).

Uninucleate amoebae as small

as 3.6/* in diameter; multinucleate forms 20-25/* 8-11/* in diameter; in the space

by

10-15/*; cysts

between the peritrophic membrane

and the epithelium of the gut in the larvae of Trichocera hiemalis, T. annulata, and T. regelationis (winter gnats). Genus Schizamoeba Davis. Nucleus vesicular, without endosome, but with large discoid granules arranged along nuclear membrane; 1 to many nuclei; cyst-nuclei formed by fragmentation of those of the trophozoite and possess a large rounded chromatic endosome, connected at one side with the nuclear membrane by achromatic

464

PROTOZOOLOGY
fish.

strands to which chromatin granules are attached; in stomach of

salmonid
ameter;
1

One
D.

species (Davis, 1926).

amoeba; 10-25/* in diby binary fission; nuclear division amitotic. Cysts are said to be more abundant than trophozoites and their appearance seems to be correlated with the amount
S. salmonis
(Fig. 198, d, e). Sluggish

to several nuclei; multiplication

of available food; cysts spherical, 15-35/t in diameter; cyst-mem-

brane thin and nuclei vary from 3 to many; during encystment, chromatin bodies of trophozoite become collected in several masses which then break up and each chromatin grain becomes the endosome of newly formed nucleus; cyst contents divide sooner or later into 4-11 multinucleate bodies and the whole increases in size; finally cyst-membrane disintegrates and the multinucleate bodies become set free. Trophozoites are said to occur in the mucous covering of stomach of host fish; cysts occur in both stomach and intestine. Aside from the loss of certain amount of available food, no pathogenic effect of the amoeba upon the host fish was noticed
(Davis).

Genus Hydramoeba Reynolds and Looper. Nucleus vesicular with a large central endosome composed of a centriole (?) and chromatin granules embedded in an achromatic mass, achromatic

membrane; a ring made up of numerous rod-shaped chromatin bodies in the nuclear-sap zone; 1 or more contractile vacuoles; apparently the most primitive parasitic amoeba; parasitic on Hydra. H. hydroxena (Entz) (Fig. 198, f-l). Parasitic in various species of Hydra; first observed by Entz; Wermel found 90 per cent of Hydra he studied in Russia were infected by the amoeba; Reynolds and Looper (1928) stated that infected Hydra die on an average in 6.8 days and that the amoebae disappear in 4-10 days if removed from a
strands radiating from endosome to

host hydra.
ules in

More

or less spheroidal, with blunt pseudopods; 60-

380/i in diameter; nucleus

life;

shows some 20

refractile peripheral gran-

contractile vacuoles; food vacuoles contain host cells;

multiplication

by binary

fission.

Hydra japonica, H. magnipapilPalmathydra robusta, etc. in Japan. The trophozoites measured 26-2 10m long with a nucleus, 10-12/x in diameter. Early infection occurs on the tip of tentacles and spreads to the body proper (Fig. 198, i-l). Since the tentacles remain contracted, the host hydra cannot feed on food organisms and becomes "depressed." The amoebae finally enter the coelenteric cavity and feed on the endoderm cells. The host hydra becomes spherical. At25C. death of the hydra may
Ito (1949) found this organism in
lata,

AMOEBINA

465

occur in one week. Encystment takes place soon after the death of the host or occasionally when the organisms become detached from
the host; cysts are spherical, measure 27.5-29m, and contain one or more nuclei, nematocysts and a large vacuole (h). Nuclear division

(Reynolds and Threlkeld, 1929).

Fig. 198. a-c, Dobellina mesnili (Bishop and Tate) (a, b, stained uniand multi-nucleate trophozoites, X2200; c, a stained cyst with six nuclei, X1760); d, e, stained trophozoite and cyst of Schizamoeba salmonis, X1070 (Davis); f-1, Hijdramoeba hydroxena (f, h-1, Ito; g, Reynolds and Looper) (f, a trophozoite in life, X330; g, a trophozoite feeding on ectodermal cells of a Hydra in section, X470; h, a living cyst, X530; i-1, stages of infection in Hydra, X6.5); m, Paramoeba pigmentifera with its

nucleus in center,

X800

(Janicki).

Family 4 Paramoebidae Poche

Genus Paramoeba Schaudinn. The amoeba possesses a nucleus and

nucleus-like secondary cytoplasmic structure, both of which multiply

by

division simultaneously; free-living or parasitic.

P. pigmentifera (Grassi) (Fig. 198, m).

About

30/x long; sluggish;

466

PROTOZOOLOGY

cytoplasm distinctly differentiated; secondary body larger than the nucleus; flagellated swarmers are said to occur; parasitic in coelom of Chaetognatha such as Sagitta claparedei, Spadella bipunctata, S. inflata, and S. serratodentata. Cytology (Janieki, 1928, 1932). P. schaudinni Faria, da Cunha and Pinto. About 7-22/x in diameter; in salt water; Rio de Janeiro, Brazil.
References

Andresen, N.: (1942) Cytoplasmic components

in the amoeba, Chaos chaos L. C. R. Lab. Carlsberg, Ser. chim., 24: 139. Angerer, C. A.: (1942) The action of cupric chloride on the proto-

plasmic viscosity of Amoeba dubia. Physiol. Zool., 15:436. Balamuth, W. and Brent, M. M.: (1950) Biological studies on

Entamoeba histolytica. IV. Proc. Soc. Exper. Biol. Med., 75:374. Barret, H. P. and Smith, Nanine M.: (1924) The cultivation of an Endamoeba from the turtle, Chelydra serpentina. Am. J. Hyg.,
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Becker, E. R.
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(1926)

Endamoeba

citelli sp.

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Burks, C. and Kaleita, E.: (1946) Cultivation of Endamoeba histolytica in artificial media from cysts in drinking water subjected to chlorination. Am. J. Trop. Med., 26:783. Belda, W. H.: (1942) Permeability to water in Pelomyxa carolinen-

Salesianum, 37:68. (1942a) II. Ibid., 37:125. (1943) III. Ibid., 38:17. Bishop, Ann: (1932) Entamoeba aulastomi. Parasitology, 24:225. (1937) Further observations upon Entamoeba aulastomi. Ibid., 29:57. and Tate, P.: (1939) The morphology and systematic position of Dobellina mesnili, etc. Ibid., 31:501. Bundesen, H. N., Conolly, J. I. et al.: (1936) Epidemic amebic dysentery: etc. Nat. Inst. Health Bull., no. 166. Carini, A.: (1933) Parasitisme des Zellerielles par des microorganismes nouveaux (Brumptina n.g.). Ann. Parasit., 11:297. (1943) Novas observacoes em batraquios e ofidios, etc. Arqu. Biol., 27:1. and Reichenow, E.: (1935) Ueber Amoebeninfektion in Zelleriellen. Arch. Protist., 84:175. Casagrandi, 0. and Barbagallo, P.: (1895) Ricerche biologiche e clinique suh" Amoeba coli. I, II. Nota prelim. Bull. Accad. Gioenia Sc. Nat. Catania, 39:4 and 41:7. Cash, J.: (1905) The British freshwater Rhizopoda and Heliozoa. 1.
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London.

Chalkley, H. W.: (1936) The behavior

of the karyosome and the "peripheral chromatin" during mitosis, etc. J. Morphol., 60:13. and Daniel, G. E.: (1933) The relation between the form of the living cell and the nuclear phases of division in Amoeba proteus. Physiol. Zool., 6:592.

AMOEBINA
Endamoeba

467

Chen, T. T. and Stabler, R. M.: (1936) Further studies on the

parasitizing opalinid ciliates. Biol. Bull., 70:72. and Sanders, E. P.: (1930) Encystation, multiple fission without encystment, excvstation, etc. Arch. Protist., 70: 223. Craig, C. F.: (1934) Amebiasis and amebic dysentery. Springfield,

Cleveland,

L. R.

111.

P. A.: (1900) Etude de la karyokinese chez V Amoeba Le Bot., Ser. 7:49. Daniels, E. W.: (1951) Studies on the effect of x-irradiation upon Pelomyxa carolinensis with special reference to nuclear division

Dangeard,

hyalina.

J. Exper. Zool., 117:189. (1952) Some effects on cell division in Pelomyxa carolinensis following x-irradiation, etc. Ibid., 120:509. (1952a) Cell division in the giant amoeba, Pelomyxa carolinensis, following x-irradiation. I. Ibid., 120:525. Davis, H. S.: (1926) Schizamoeba salmonis, a new ameba parasitic in salmonid fishes. Bull. Bur. Fisheries, 42, 8 pp. Dawson, J. A.: (1945) Studies on the contractile vacuole of Amoeba dubia. J. Exper. Zool., 100:179. Kessler, W. R. and Silverstein, J. K.: (1935) Mitosis in Amoeba dubia. Biol. Bull, 69:447. Dobell, C: (1918) Are Entamoeba histolytica and E. ranarum the same species? Parasitology, 10:294. (1919) Amoebae living in man. London. (1928) Researches on the intestinal Protozoa of monkeys and man. I, II. Parasitology, 20:359. (1938) IX. Ibid., 30:195. (1940) X. Ibid., 32:417. (1943) XI. Ibid., 35:134. and O'Connor, F. W. (1921) The intestinal Protozoa of

and plasmotomy.

man. London. Douglas, M.: (1930) Notes on the classification of the amoeba, etc. J. Trop. Med. Hyg., 33:258. Entz, G. Jr.: (1912) Ueber eine neue Amoebe auf Susswasser-Polypen {Hydra oligactis). Arch. Protist., 27:19. Geiman, Q. M. and Ratcliffe, H. L.: (1936) Morphology and lifecycle of an amoeba producing amoebiasis in reptiles. Parasitology, 28:208.

Greeff, R. (1874) Pelomyxa palustris (Pelobius), ein amoebenartiger Organismus des siissen Wassers. Arch. mikr. Anat., 10:53. Groot, A. A. de: (1936) Einige Beobachtungen an Dinamoeba mira:

bilis.

Arch. Protist., 87:427.

Gutierrez-Ballesteros, E. and Wenrich, D. H.: (1950) Endolimax clevelandi, n. sp. from turtle. J. Parasit., 36:489. Hardy, A. V. and Spector, B. K.: (1935) The occurrence of infestations with E. histolytica associated with water-borne epidemic diseases. Publ. Health Rep. Washington, 50:323. Hartmann, M. and Chagas, C.: (1910) Ueber die Kernteilung von Amoeba hyalina. Mem. Inst. Oswaldo Cruz, 2:159.

468

PROTOZOOLOGY

Hegner, R. W.: (1926) Endolimax caviae, etc. J. Parasit., 12:146. Hemming, F.: (1951) Report on the investigation of the nomenclau torial problems associated with the generic names Endamoeba^
etc. Bull. Zool.
J.

Nomenclature, 2:277.

Henderson,
of the

some amoebae from a termite genus Cubitermes. Univ. California Publ. Zool., 43:357. Hewitt, R.: (1937) The natural habitat and distribution of Hartmannella castellanii, etc. J. Parasit., 23:491. Hoare, C. A.: (1940) On an Entamoeba occurring in English goats.
(1941) Studies of

C:

Parasitology, 32:226. J.: (1921) Studies on the life history of Vahlkampjla patuxent, etc. Am. J. Hyg., 1:321. Hollande, A.: (1945) Biologie et reproduction des rhizopodes des genres Pelomyxa et Amoeba, etc. Bull. Biol. France et Belg., 79:31. Hyman, Libbie H.: (1936) Observations on Protozoa. I. Quart. J. Micr. Sc, 79:43. Ito, T. (1949) On Hydramoeba hydroxena discovered in Japan. Sc. Rep. Tohoku Univ., Ser. 4, 18:205. Janicki, C: (1928) Studien an Genus Paramoeba Schaud. Neue Folge. I. Zeitschr. wiss. Zool., 131:588. (1932) II. Ibid., 142:587. Jepps, Margaret W. and Dobell, C: (1918) Dientamoeba fragilis, Parasit., 10:352. etc. Jollos, V. (1917) Untersuchungen zur Morphologie der Amoebenteilung. Arch. Protist., 37:229. Keller, H.: (1949) Untersuchungen iiber die intrazellularen Bakterien von Pelomyxa palustris. Ztschr. Naturforsch., 46:293. Kirby, H. Jr.: (1927) Studies on some amoebae from the termite Microtermes, etc. Quart. J. Micr. Sc, 71:189. (1945) Entamoeba coli versus Endamoeba coli. J. Parasit., 31

Hogue, Mary

177.

Koch, D. A.: (1927) Relation of moisture and temperature to the viability of Endamoeba gingivalis in vitro. Univ. California
Publ. Zool., 31:17.

Kofoid, C. A. and Johnstone, H. G.: (1930) The monkeys. Ibid., 33:379. Kudo, R. R. (1926) Observations on Endamoeba
:

oral

amoeba

of
J.

blattae.

Am.
J.

Hyg., 6:139. (1926a) Observations on Dientamoeba

fragilis.

Am.

Trop.

I. Jour. Morph., 78: 317. (1947) II. Ibid., 80:93. (1949) III. Ibid., 85:163. (1950) species of Pelomyxa from Illinois. Tr. Am. Micr.

Med., 6:299. (1946) Pelomyxa carolinensis Wilson.

Soc, 69:368. (1951) Observations on Pelomyxa

88:145.

illinoisensis. Jour.

Morph.,
:

(1952)

The genus Pelomyxa.

Tr.

Am.

Micr. Soc, 71

108.

AMOEBINA

469

Kuenen, W. A. and Swellengrebel, N. H.: (1913) Die Entamoeben des Menschen und ihre praktische Bedeutung. Centralbl.
Bakt.
I.

Orig., 71:378.

Lapage, G.: (1922) Cannibalism in Amoeba vespertilio. Quart. J. Micr. Sc, 66:669. Leidy, J.: (1879) Freshwater rhizopods of North America. Rep. U. S. Geol. Survey Terr., 12. Liesche, W.: (1938) Der Kern- und Fortpflanzungsverhaltnisse von

Amoeba

proteus. Arch. Protist., 91:135.

:

Two new species of amoeba found in cockroaches: etc. Parasitology, 19:223. Mackinnon, Doris L. and Ray, H. N.: (1931) An amoeba from the intestine of an ascidian at Plymouth. J. Mar. Biol. Ass. United
Lucas, Catherine L. T. (1927)

Kingdom, 17:583. and Dibb, M. J.: (1938) Report on intestinal Protozoa of some mammals, etc. Proc. Zool. Soc. London, B, 108:323. Mast, S. 0.: (1926) Structure, movement, locomotion and stimulation in Amoeba. J. Morphol., 14:347. (1934) Amoeboid movement in Pelomyxa palustris. Physiol.
Zool., 7:470.

(1938)

Amoeba and Pelomyxa

vs.

Chaos. Turt. News, 16:

56.

and Doyle, W. L.: (1935) Structure, origin and function of cytoplasmic constituents in Amoeba proteus. I. Arch. Protist., 86:155. (1935a) II. Ibid., 86:278. and Johnson, P. L.: (1931) Concerning the scientific name of the common large amoeba, usually designated Amoeba proteus. Ibid., 75:14. Meglitsch, P. A.: (1940) Cytological observations on Endamoeba
blattae. Illinois Biol.

Mercier,
tist.,

L.: (1909)

Le

Monogr., 14: no. 4. cycle evolutif d' Amoeba blattae. Arch. Problattae. J.

16:164.
S.: (1936)
J.:

Morris,
225.

Studies of Endamoeba
(1950)

Morphol., 59:

Musacchia, X.

Encystment

in

Pelomyxa

carolinensis. St.

Louis "Univ. Stud., Sec. C, 1, 6 pp. Nie, D.: (1950) Morphology and taxonomy of the intestinal Protozoa of the guinea-pig, Cavia porcella. J. Morphol., 86:381.

Nieschulz, O.: (1924) Ueber Entamoeba

deblicki mihi, eine

Darm-

amoebe des Schweines. Arch. Protist., 48:365. Noble, E. R.: (1947) Cell division in Entamoeba gingivalis. Univ.
California Publ. Zool., 53:263. (1950) On the morphology of Entamoeba bovis. Ibis., 57:341. Noble, G. A. and Noble, E. R.: (1952) Entamoebae in farm mammals. J. Parasit., 38:571. Okada, Y. K. (1930) Transplantationsversuche an Protozoen. Arch. Protist., 69:39. (1930a) Ueber den Bau und die Bewegungsweise von
:

Pelomyxa.

Ibid., 70:131,

470

PROTOZOOLOGY

Penard,

E.: (1902) Faune rhizopodique du bassin du Leman. Geneva. Raabe, H.: (1951) Amoeba vespertilio Penard; etc. Bull. Int. Acad.
Pol. Sci. et Lett., Ser. B., p. 353.
J.

(1947) Cytological observations on the amoeboNaegleria gruberi. J. Morphol., 81:1. Ratcliffe, H. L. and Geiman, Q. M.: (1938) Spontaneous and experimental amebic infection in reptiles. Arch. Path., 25:160. Reynolds, B. D. and Looper, J. B. (1928) Infection experiment with Hydr amoeba hydroxena. J. Parasit., 15:23. and Threlkeld, W. L.: (1929) Nuclear division in Hydramoeba hydroxena. Arch. Protist., 68:305. Rice, N. E.: (1945) Pelomyxa carolinensis (Wilson) or Chaos chaos (Linnaeus)? Biol. Bull., 88:139. Rodhain, J.: (1934) Entamoeba invadens n. sp., etc. C. R. Soc. Biol., 117:1195. Root, F. M.: (1921) Experiments on the carriage of intestinal Protozoa of man by flies. Am. J. Hyg., 1:131. Sanders, Elizabeth P.: (1931) The life-cycle of Entamoeba ranarum. Arch. Protist., 74:365. and Cleveland, L. R.: (1930) The morphology and life-cycle of Entamoeba terrapinae, etc. Ibid., 70:267. Schaeffer, A. A.: (1916) Notes on the specific and other characteristics of Amoeba proteus, etc. Ibid., 37:204. (1926) Taxonomy of the amebas. Papers Dep. Mar. Biol.,
S.: flagellate,
:

Rafalko,

Carnegie Inst. Washington, 24. (1937) Rediscovery of the giant ameba of Roesel,

etc.

Turt.

News, 15:114.
(1938)
Significance
of

3-daughter division in the giant

amoeba. Ibid., 16:157. Schaudinn, F.: (1896) Ueber den Zeugungskreis von Paramoeba eilhardi, etc. Math, naturwiss. Mitt., 1:25. (1903) Untersuchungen ueber die Fortpflanzung einiger Rhizopoden. Arb. kaiserl. Gesundh.-Amte, 19:547. Singh, B. N.: (1952) Nuclear division in nine species of small freeliving amoebae, etc. Phil. Tr. Roy. Soc. London, Ser. B, 236:
405.

Snyder, T. L. and Meleney, H. E.: (1941) The excystation Endamoeba histolytica in bacteriologically sterile media. Am. Trop. Med., 21:63. Stabler, R. M.: (1940) Binary fission in Entamoeba gingivalis.
Morphol., 66:357.

of
J.

J.

Chen, T. T. (1936) Observations on an Endamoeba parasitizing opalinid ciliates. Biol. Bull., 70:56. Taliaferro, W. H. and Holmes, F. O.: (1924) Endamoeba barreti,
:

and

etc.

Am.

J.
:

Hyg., 4:155.
of the caeca of the

Tyzzer, E. E. (1920) Amoebae

common
etc.

fowl and

of the turkey. J. Med. Res., 41:199. Volkonsky, M.: (1931) Hartmannella castellanii,

Arch. zool.

exper. gen., 72:317.

AMOEBINA
Walker,

471

E. L.: (1908) The parasitic amoebae of the intestinal tract of man and other animals. J. Med. Res., 17:379. Wenrich, D. H. (1936) Studies on Dientamoeba fragilis. I. Jour. Parasit., 22:76. (1937) II. Ibid., 23:183. (1937a) Studies on Iodamoeba butschlii with special reference to nuclear structure. Proc. Am. Philos. Soc, 77:183. (1939) Studies on Dientamoeba fragilis. III. J. Parasit., 25:
:

43.

(1940) Nuclear structure and nuclear division in the trophic stages of Entamoeba muris. J. Morph., 66:215. (1941) Observations on the food habits of Entamoeba muris

and Entamoeba ranarum. Biol. Bull., 81:324. (1944) Studies on Dientamoeba fragilis. IV.

J.

Parasit.,

30:322. (1944a) Nuclear structure and nuclear division in Dientamoeba fragilis. J. Morph., 74:467. Wenyon, C. M.: (1926) Protozoology. 1. London and Baltimore. Wermel, E.: (1925) Beitrage zur Cytologie der Amoeba hydroxena Entz. Arch. russ. Protist., 4:95. Wilber, C. G.: (1942) The cytology of Pelomyxa carolinensis. Tr. Am. Micr. Soc, 61:227. (1945) Origin and function of the protoplasmic constituents in Pelomyxa carolinenesis. Biol. Bull., 88:207. (1946) Notes on locomotion in Pelomyxa carolinensis. Tr. Am. Micr. Soc, 65:318. (1947) Concerning the correct name of the rhizopod, Pelomyxa carolinensis. Ibid., 66:99. Wilson, H. V.: (1900) Notes on a species of Pelomyxa. Am. Nat., 34:535. Yorke, W. and Adams, A. R. D.: (1926) Observations on Entamoeba histolytica. I. Ann. Trop. Med. Parasit., 20:279.

Chapter 20

Order 4 Testacea Schultze

Testacea or Thecamoeba comprise those amoeboid organTHE within which or enveloped by a simple isms which
are
shell
test,

body can be completely withdrawn. The shell has usually a single aperture through which pseudopodia protrude, and varies in shape and structure, although a chitinous or pseudochitinous membrane forms the basis of all. It may be thickened, as in Arcella and others, or composed of foreign bodies cemented together as in Difflugia, while in Euglypha siliceous platelets or scales are formed in the endoplasm and deposited in the shell. The cytoplasm is ordinarily differentiated into the ectoplasm and endoplasm. The ectoplasm is conspicuously observable at the aperthe
ture of the shell where filopodia or slender ectoplasmic lobopodia
are produced.

The endoplasm

is

tains food vacuoles, contractile vacuoles

granulated or vacuolated and conand nuclei. In some forms

there are present regularly in the cytoplasm

numerous basophilic

granules which are

known

as 'chromidia' (p. 44).

Asexual reproduction is either by longitudinal fission in the forms with thin tests, or by transverse division or budding, while in others multiple division occurs. Encystment is common. Sexual reproduction by amoeboid or flagellate gametes has been reported in some
species.

The

testaceans are mostly inhabitants of fresh water, but

some

water and others are semi-terrestrial, being found in moss or moist soil, especially peaty soil. Biology of soil-inhabiting forms (Volz, 1929); ecology (Hoogenraad, 1935).
live in salt

Shell simple and membranous Filopodia, in some anastomosing

Pseudopodia

fllose,

simply branched

Family 1 Gromiidae Family 2 Arcellidae (p. 476)

Shell with foreign bodies, platelets, or scales

With With

foreign bodies
platelets or scales

Family 3 Difflugiidae Family 4 Euglyphidae

(p. (p.

482) 487)

Family

Gromiidae Eimer and Fickert

in the Foraminifera

These forms are frequently included

authors.

by other
Diplo-

Genus Gromia Dujardin (Allogromia,

Rhynchogromia,

gromia Rhumbler). Thin test rigid or flexible, smooth or slightly coated with foreign bodies; spherical to elongate ellipsoid; aperture
472

TESTACEA
terminal;
1

473

or more nuclei; contractile vacuoles;

many

filopodia,

branching and anastomosing; cytoplasm with numerous motile

granules; fresh or salt water.

Many species.
smooth

G.fluvialis D. (Fig. 199, a). Test spherical to subspherical;

or sparsely covered with siliceous particles; yellowish cytoplasm

fills

the test; aperture not seen; a large nucleus and numerous con-

tractile vacuoles; filopodia long, often

enveloping test; 90-250/*

long;

on aquatic

plants, in

moss or

soil.

G. ovoidea (Rhumbler) (Fig. 199, b). In salt water. G. nigricans (Penard) (Fig. 199,
c).

section; a single nucleus; 220-400/* long; in

tation.

Test large, circular in crosspond water among vege-

Genus Microgromia Hertwig and

Lesser. Test small, hyaline,

spherical or pyriform, not compressed; aperture terminal, circular;

filopodia long straight or anastomosing, arising
single nucleus

and

contractile vacuole; solitary or grouped.

from a peduncle; a Morphol-

ogy (Valkanov, 1930).

M.

socialis (Archer) (Fig. 199, d).

Cytoplasm bluish; contractile

vacuole near aperture; filopodia arise from a peduncle, attenuate,

branching, anastomosing; often numerous individuals are grouped;

by fission and also by swarmers; 25-35/* in diameter; among vegetation in fresh water. Genus Microcometes Cienkowski. Body globular, enclosed within
multiplication

a transparent, delicate, light yellowish and pliable envelope with 3-5 apertures, through which long branching filopodia extend; body protoplasm occupies about 1/2 the space of envelope; 1-2 contractile

vacuoles fresh
;

w ater.
e).

M.
water

paludosa C. (Fig. 199,

About

16-17/* in diameter; fresh

among algae (Valkanov,

1931; Jepps, 1934).

Genus Artodiscus Penard. Body globular, plastic; covered by envelope containing small grains of various kinds; nucleus eccentric;
a few pseudopodia extend through pores of the envelope; movement very rapid fresh water. A. saltans P. (Fig. 199,/). 18-23/* in diameter; fresh water. Genus Lieberkiihnia Claparede and Lachmann. Test ovoidal or spherical, with or without attached foreign particles; aperture usually single, lateral or subterminal; one or more nuclei; many contractile vacuoles; pseudopodia formed from a long peduncle, reticulate, often enveloping test; fresh or salt water. L. wagneri C. and L. (Fig. 200, a). Spheroidal; aperture subtermi;

nal, oblique, flexible; cytoplasm slightly yellowish, fills the test; 80-150 vesicular nuclei; nuclei 6/* in diameter; many contractile vac-

474

PROTOZOOLOGY

X120 (Dujardin); b, (?. ovoidea, X50 X200 (Cash and Wailes); d, Microgromia socialis, X170 (Cash); e, Microcometes paludosa, X670? (Penard); f, Artodiscus saltans, X670 (Penard); g, Schultzella diffluens, X120
a,

Fig. 199. (Schultze);

Gromia

fluvialis,

c,

(r.

nigricans,

(Rhumbler).

TESTACEA
uoles; pseudopodia long, anastomosing; 60-1 60m long;
in fresh

475

among

algae

and

salt water.

thin, spherical; 2 apertures, one cytoplasm colorless; a single nucleus; several contractile vacuoles; filo podia radiating. One species. D. archeri B. (Fig. 200, b). With 1-3 colored oil droplets; pseudopodia highly attenuate, radiating, straight or branched; multiplication into 2 or 4 daughter individuals; solitary or in groups; diameter 8-20/z; on submerged plants in fresh water.

Genus Diplophrys Barker. Test

at each pole;

b, Diplophrys Lecythium hyalinum, X330 (Cash and Wailes); d, Myxotheca arenilega, X70 (Schaudinn); e, Dactylosaccus vermiformis, Xl5 (Rhumbler); f, Boderia turneri (Wright).

Fig. 200.

a,

Lieberkuhnia ivagneri,

X160 (Verworn);
c,

archeri,

X930 (Hertwig and

Lesser);

Genus Lecythium Hertwig and

less;

Lesser. Test thin, flexible, colorfills

aperture elastic, terminal; colorless cytoplasm

the test;

large nucleus posterior;

numerous

filopodia long, branching, not

anastomosing; fresh water. L. hyalinum (Ehrenberg) (Fig. 200, c). Spheroidal; aperture circular with a short flexible neck; a single contractile vacuole; diameter 20-45/z
;

in

submerged vegetation.

476

PROTOZOOLOGY

Genus Schultzella Rhumbler. Test thin, delicate, difficult to life, easily broken at any point for formation of pseudopodia which branch and anastomose; irregularly rounded; without
recognize in
foreign material; salt water.
S. diffluens (Grubler) (Fig. 199, g).

opaque, colorless; with

nuclei
;

oil

droplets, vacuoles

Cytoplasm finely granulated; and numerous small

up to 220/j. in diameter. Genus Myxotheca Schaudinn. Amoeboid; spherical or hemispherical, being flattened on the attached surface; a thin pseudochitinous test with foreign bodies, especially sand grains; pseudo-

podia anastomosing;

salt water.

Nucleus (Foyn, 1936).

M.

arenilega S. (Fig. 200, d). Test yellow, with loosely attached

foreign bodies; cytoplasm bright red due to the presence of highly

refractile granules; 1-2 nuclei, 39-75ju in diameter;

body diameter

160-560/z.

Genus Dactylosaccus Rhumbler. Test sausage-shape and variously twisted; pseudo podia filiform, anastomosing; salt water.
D. vermiformis R. (Fig. 200,
e).

from small
salt water.

finger-like projections; 1-2 nuclei;

Test smooth; pseudo podia rise body 4 mm. by 340m

Genus Boderia Wright. Body form changeable; often spherical, but usually flattened and angular; filopodia long; test extremely
delicate, colorless; salt water.

B. turneri W. (Fig. 200, /). Body brown to orange; active cytoplasmic movement; 1-10 nuclei multiple division(?) 1.56-6.25 mm.
; ;

in

diameter; in shallow water.

Family 2 Arcellidae Schultze

Genus Arcella Ehrenberg. Test transparent, chitinous, densely punctated; colorless to brown (when old); in front view circular,
angular, or stellate; in profile plano-convex or semicircular; vari-

ously ornamented; aperture circular, central, inverted like a funnel; protoplasmic body does not fill the test and connected with the latter

by many ectoplasmic strands; slender lobopodia, few, digitate, simple or branched; 2 or more nuclei; several contractile vacuoles; fresh water. Numerous species. Taxonomy and morphology (Deflandre, 1928); variation and heredity (Jollos, 1924).
ter;

A. vulgaris E. (Fig. 201, a, b). Height of test about 1/2 the diamedome of hemispherical test evenly convex; aperture circular, central; colorless, yellow, or brown; protoplasmic body conforms with the shape of, but does not fill, the test; lobopodia hyaline; 2
vesicular nuclei; several contractile vacuoles; test 30-100/x in dia-

TESTACEA

477

meter; in the ooze and vegetation in stagnant water and also in soil. Of several varieties, two may be mentioned; var. angulosa (Perty),

forming a 5- to 8-sided with obtuse angles; var. gibbosa (Penard), test gibbous, surface pitted with circular depressions of uniform dimensions: 45-50xi
test smaller, 30-40/i in diameter, faceted,
figure,

up to

100/z in diameter.

x^cSW

Fig. 201. a, b, Arcella vulgaris, X170; X230 (Leidy); c, A. discoides, (Leidy); d, A. mitrata, X140 (Leidy); e, f, A. catinus. X 170 (Cash); g-i, A. dentata, X170 (Leidy); j, k, A. artocrea, X170 (Leidy).

X170

A. discoides E. (Fig. 201, c). Test circular in front view, planoconvex in profile; diameter about 3-4 times the height; test coloration and body structure similar to those of A. vulgaris; test 70260/t in diameter; in fresh water.

A. mitrata Leidy (Fig. 201,

d).

Test balloon-shaped or polyhedral;

height exceeds diameter of base; aperture circular, crenulated and

usually evarted within inverted funnel; protoplasmic
roidal,

body sphetest; 6 or

with 'neck' to aperture and cytoplasmic strands to

more slender lobopodia;

in fresh

test 100-145/* high, 100-152/* in diameter;

water among vegetation. A. catinus Penard (Fig. 201, e, /). Test oval or quadrate, not circular, in front view; aperture oval; dome compressed; lateral margin with 6 or 8 facets; test 100-120/i in diameter and about 45/i high; fresh water among vegetation. A. dentata Ehrenberg (Fig. 201, g-i). Test circular and dentate

478

PROTOZOOLOGY
diameter more than twice the

in front view, crown-like in profile;

height; aperture circular, large; colorless to brown; about 95^ in

diameter, aperture 30/x in diameter; 15-17 spines; in the ooze of

freshwater ponds.
ter;

A. artocrea Leidy (Fig. 201, j, k). Heightof test 1/4-1/2 the diamedome convex; surface mammillated or pitted; border of test everted and rising 1/4-1/2 the height of test; about 175/z in diameter; fresh water.

a, b, Pyxidicula operculata, X800 (Penard); c, Pseudochlamys X330 (Cash); d, e, Difflugiella apicidata, X270 (Cash); f, Cryptodifflugia oviformis, X320 (Cash); g, Lesquereusia spiralis, X270 (West); h, Hyalosphenia papilio, X330 (Leidy); i, Corycia coronata, X170 (Penard); j, Pamphagus mutabilis, X330 (Leidy); k, Plagiophrys parvipunctata, X330 (Penard).

Fig. 202,

patella,

Genus Pyxidicula Ehrenberg. Test patelliform; rigid, transparent, punctate; aperture circular, almost the entire diameter of test; cytoplasm similar to that of Arcella; a single nucleus; 1 or more
contractile vacuoles; fresh water.

P. operculata (Agardh) (Fig. 202,

a, b).

brown; a

single vesicular nucleus;

Test smooth, colorless to pseudopodia short, lobose or

digitate; 20/x in diameter;

on vegetation.

TESTACEA
flexible

479

Genus Pseudochlamys Claparede and Lachmann. Test discoid, when young; body with a central nucleus and several conP. patella C. and L. (Fig. 202,

tractile vacuoles.
c). Young test hyaline, older one and brown; often rolled up like a scroll; a short finger-like pseudopodium between folds; 40-45ai in diameter; in fresh water among vegetation, in moss and soil. Genus Difflugiella Cash. Test ovoid, not compressed, flexible and transparent membrane; colorless cytoplasm fills the test, usually with chlorophyllous food material; median pseudopodia lobate or digitate with aciculate ends, while lateral pseudopods long, straight, and fine, tapering to a point; fresh water. One species.

rigid

D. apiculata C. (Fig. 202,

tation.

d, e).

About 40^ by

28/z;

among

vege-

Genus Cryptodifflugia Penard. Small

test j^ellowish to

Difflugia-like in general appearance, compressed; with or

brownish; without

foreign bodies; pseudopodia long, acutely pointed; fresh water.

C. ovijormis P. (Fig. 202, /). Test ovoid; without foreign bodies;

crown hemispherical; aperture truncate; cytoplasm with chlorophyllous food particles; 16-20/x by 12-15/x; in marshy soil. Genus Lesquereusia Schlumberger. Test compressed, oval or globular in profile, narrowed at bent back; semispiral in appearance; with curved or comma-shaped rods or with sand-grains (in one species); body does not fill up the test; pseudopodia simple or branched fresh water.
;

L. spiralis (Ehrenberg) (Fig. 202, g). Aperture circular; border

distinct;

cytoplasm appears pale yellow; a single nucleus; 96-188/x

;

by 68-1 14/i in marsh water. Genus Hyalosphenia Stein. Test ovoid or pyriform; aperture end convex; homogeneous and hyaline, mostly compressed; crown uniformly arched; protoplasm partly filling the test; several blunt pseudopodia simple or digitate. Several species.

H. papilio Leidy (Fig. 202, h). Test yellowish; transparent; pyriform or oblong in front view a minute pore on each side of crown and sometimes one also in center; aperture convex; in narrow lateral
;

view, elongate pyriform, aperture a shallow notch; with chloro-

phyllous particles and oil globules; 110-140/* long; in fresh water

among

vegetation.
pliable,

Genus Corycia Dujardin. Envelope extremely

base, but

open at

changes its shape with movement and contraction of body; with or without spinous pro-

when

closed, sack-like; envelope

jections.

480
C. coronata
in moss.

PROTOZOOLOGY
Penard
(Fig. 202,
i).

6-12 spines;

140/* in

diameter;
flexible;

Genus Pamphagus Bailey. Test hyaline membranous,

aperture small; body
fills

the envelope completely; spherical nuc-

filo podia long, delicate, branching, but not anastomosing; fresh water. Species (Hoogenraad, 1936). P. mutabilis B. (Fig. 202, j). Envelope 40-100/* by 28-68/*. Genus Plagiophrys Claparede and Lachmann. Envelope thin, hyaline, changeable with body form; usually elongate-oval with rounded posterior end; narrowed at other half; envelope finely punctated with a few small plates; aperture round; cytoplasm

leus large; contractile vacuoles;

clear; nucleus large; pseudopods straight branching fresh water.

;

filopodia,

sometimes

P. parvipunctata Penard (Fig. 202, k). Envelope 50/* long. Genus Leptochlamys West. Test ovoid, thin transparent chitinous membrane, circular in optical section; aperture end slightly expanded with a short neck; aperture circular, often oblique; body fills test; without vacuoles; pseudo podium short, broadly expanded and sometimes cordate; fresh water.
L. ampullacea

W.

(Fig. 203, a).

Nucleus

large, posterior;

with

green or brown food particles; test 45-55/* by 36-40/* in diameter;

aperture 15-17/*;

among

algae.

Genus Chlamydophrys Cienkowski. Test rigid, circular in crosssection; aperture often on drawn-out neck; body fills the test; zonal
differentiation of cytoplasm distinct; nucleus vesicular; refractile

waste granules; pseudopodia branching; fresh water or coprozoic.

Species (Belaf, 1926); plasmogamy and division (Belar, 1926). C. stercorea C. (Fig. 203, k). Test 18-20/* by 12-15/*; mature cysts

yellowish brown, 12-15/* in diameter; multiplication

by budding;

coprozoic and fresh water.

Genus Cochliopodium Hertwig and

Lesser. Test thin, flexible,

expansible and contractile; with or without extremely fine hair-like

processes; pseudopodia blunt or pointed, but not acicular. Several
species.

C. bilimbosum (Auerbach) (Fig. 203, b). Test hemispherical; pseudopodia conical with pointed ends; test 24-56/* in diameter; fresh water among algae. Genus Amphizonella Greeff. Test membranous with a double marginal contour; inner membrane smooth, well-defined; outer serrulate; aperture inverted; a single nucleus; pseudopodia blunt,
digitate,

and divergent.
c).

A. violacea G. (Fig. 203,

Test patelliform, violet-tinted; with

TESTACEA
160/z; fresh

481

chlorophyllous corpuscles and grains; sluggish; average diameter

water.
Ntisslin.

Genus Zonomyxa

chitinous, violet-colored;

Test rounded pyriform, flexible, endoplasm vacuolated, with chlorophyl-

bilimbosum,
d,

Fig. 203. a, Leptochlamys ampullacea, X330 (West); b, Cochliopodium X670 (Leidy); c, Amphizonella violacea, X270 (Greeff);

Zonomyxa

violacea,

X200 (Penard);

e,

f,

Microcorycia flava,

X240

(Wailes); g, h, Parmulina cyathus, X500 (Penard); i, Diplochlamys leidyi X270 (Brown); j, Capsellina timida, X270 (Wailes); k, Chlamydophrys
stercorea,

X670 (Wenyon).

lous particles; several nuclei; pseudo podia simple, not digitate; fresh

water.
Z. violacea N. (Fig. 203, d). A single lobular pseudo podium with acuminate end; 4 nuclei; diameter 140-160/u; actively motile forms 250/z or longer; among sphagnum. Genus Microcorycia Cockerell. Test discoidal or hemispherical,.

482
flexible,

PROTOZOOLOGY
with a diaphanous continuation or fringe around periphery,

being folded together or completely closed; crown of test with circular or radial ridges; body does not fill the test; 1-2 nuclei; pseu-

dopodia lobular or digitate; fresh water. A few species. M. flava (Greeff) (Fig. 203, e, /). Test yellowish brown; crown with few small foreign bodies; endoplasm with yellowish brown granules; 2 nuclei; contractile vacuoles; diameter 80-100/*; young
individuals as small as 20ju; in moss.

bodies; aperture
tile

Genus Parmulina Penard. Test ovoid, chitinoid with foreign may be closed; a single nucleus; 1 or more contracvacuoles; fresh water.

few

species.

P. cyathus P. (Fig. 203, g, h). Test small, flexible; ovoid in aperture view, semicircular in profile; aperture a long, narrow slit when
test
is

closed,

but circular or

elliptical

when opened;

40-55/* long;

in moss.

Genus Capsellina Penard. Test hyaline, ovoid, membranous; with or without a second outer covering; aperture long slit; a single nucleus; 1 or more contractile vacuoles; filose pseudopodia; fresh
water.
C. timida
section; with

Brown

(Fig.
(?)

203, j). Small, ovoid; elliptical in cross-

many oil

globules;

filo

podium;

34/*

by

25/*; in

moss.

Genus Diplochlamys
flexible

Greeff.

Test hemispherical or cup-shaped,

with a double envelope; inner envelope a membranous sack with an elastic aperture; outer envelope with loosely attached foreign bodies; aperture large; nuclei up to 100; pseudopodia few,
short, digitate or pointed; fresh water. Several species.

D.
ing

leidyi

G. (Fig. 203,

i).

beyond outer aperture; nuclei up

Test dark gray; inner envelope projectto 20 in number; diameter

80-100/*.

Family 3 Difflugiidae Taranek

Genus

Difflugia Leclerc. Test variable in shape,

circular in cross-section;

composed

of

but generally cemented quartz-sand, difills

atoms, and other foreign bodies; aperture terminal; often with

zoochlorellae; cytoplasmic
cleus;

body almost

the test; a single nusoil,

many

contractile vacuoles; pseudopodia cylindrical, simple

or branching; end rounded or pointed; fresh water, woodland

etc.

D. oblonga Ehrenberg (D. pyriformis Perty)

(Fig. 204, a).

Test

pyriform, flask-shaped, or ovoid; neck variable in length; fundus rounded, with occasionally 1-3 conical processes; aperture terminal,
typically circular; test

composed of angular sand-grains, diatoms;

bright green with chlorophyllous bodies; 60-580/*

by

40-240/*; in

TESTACEA
the ooze of fresh water ponds, ditches and bogs; also in moist
Several varieties.

483
soil.

D. urceolata Carter (Fig. 204, b). A large ovoid, rotund test, with a short neck and a rim around aperture; 200-230^ by 150-200^: in ditches, ponds, sphagnous swamps, etc.

Fig. 204. a, Difflugia oblonga, X130 (Cash); b, D. urceolata, X130 (Leidy); c, d, D. arcula, X170 (Leidy); e, D. lobostoma, X130 (Leidy); f, D. constricta, X200 (Cash); g, Centropyxis aculeata, X200 (Cash); h, Campuscus cornutus, X170 (Leidy); i, Cucurbitella mespiliformis, X200 (Wailes).

D. arcula Leidy (Fig. 204,

test yellowish

c,
;

d).

Test hemispherical, base slightly

concave, but not invaginated aperture triangular, central, trilobed

with scattered sand-grains or diatoms; diameter

swamp, moss, soil, etc. D. lobostoma L. (Fig. 204, e). Test ovoid to subspherical; aperture terminal; with 3-6 lobes; test usually composed of sand-grains, rarely with diatoms; endoplasm colorless or greenish; diameter
100-140ju; in sphagnous

80-120ju; in fresh water. Sexual fusion

and

life

cycle (Goette, 1916).

D. constricta (Ehrenberg) (Fig. 204, /). Test laterally ovoid, fundus more or less prolonged obliquely upward, rounded, and simple or provided with spines; soil forms generally spineless; aperture antero -inferior, large, circular or oval and its edge inverted; test composed of quartz grains; colorless to brown; cytoplasm colorless; 80-340/1 long; in the ooze of ponds and in soil.

484

PROTOZOOLOGY

D. corona Wallich. Test ovoid to spheroid, circular in crosscrown broadly rounded, with a variable number of spines, aperture more or less convex in profile, central and its border multidentate or multilobate; test with fine sand-grains, opaque; cytoplasm colorless; pseudopodia numerous, long, branching or bifurcating; 180-230^ by about 150^; in fresh water. Genetics (Jennings,
section;

1916, 1937).

Genus Centropyxis

Stein.

Test circular, ovoid, or discoid; aper-

ture eccentric, circular or ovoidal, often with a lobate border; with

or without spines; cytoplasm colorless; pseudopodia digitate; fresh water. Species (Deflandre, 1929).
C. aculeata S. (Fig. 204, g). Test variable in contour and size; with 4-6 spines; opaque or semitransparent with fine sand-grains or diatom shells; pseudopodia sometimes knotted or branching; when encysted, the body assumes a spherical form in wider part of test; granulated, colorless or with green globules; diameter 100-150)u;
;

aperture 50-60/z in diameter.

Genus Campascus Leidy. Test retort-shaped with curved neck, rounded triangular in cross-section; aperture circular, oblique, with
a thin transparent discoid collar; nucleus large;
tile
1

or more contrac-

vacuoles;

body does not

fill

the test; fresh water.

C. cornutus L. (Fig. 204, h). Test pale-yellow, retort-form; with a covering of small sand particles; triangular in cross-section; a single nucleus and contractile vacuole; filo podia straight; 110-140/n long; aperture 24-28ju in diameter; in the ooze of mountain lakes. Genus Cucurbitella Penard. Test ovoid with sand-grains, not compressed; aperture terminal, circular, surrounded by a 4-lobed annular collar; cytoplasm grayish, with zoochlorellae; nucleus large; 1 to many contractile vacuoles; pseudopodia numerous,
digitate; fresh water.

C. mespiliformis
105ju; in

P. (Fig. 204,

i).

115-140/* long; diameter 80in front view; ovoid cytoplasm gray, with a single

the ooze or on vegetaiton in ponds and ditches.

Genus Plagiopyxis Penard. Test subcircular

in profile; aperture linear or lunate;

nucleus and a contractile vacuole; fresh water.

P. callida P. (Fig. 205, a). Test gray, yellowish, or brown; large

nucleus vesicular; pseudopodia numerous, radiating, short, pointed

or palmate; diameter 55-135/x; in vegetation.

Genus Pontigulasia Rhumbler. Test similar to that of Difflugia, but with a constriction of neck and internally a diaphragm made of
the same substances as those of the test.
P. vas (Leidy) (Fig. 205,
b).

Round

or ovoid test; constriction

TESTACEA

485

deep and well-marked; with sand-grains and other particles; aperture terminal; 125-170/z long; fresh water ponds. Stump (1943) made a study of the nuclear division of the organism. During metaphase 8-12 "chromosomes" form a well-defined equatorial plate; average time for completion of the division was found to be 80 minutes.

Fig. 205. a, Plagiopyxis callida, X200 (Wailes); b, Pontigulasia vas X200 (Cash); c, Phnjganella acropodia, X190 (Cash); d, Bullinula indica, X130 (Wailes); e, f, Heleopera petricola, X190 (Cash); g, Nadinella tenella, X400 (Penard); h, Frenzelina reniformis, X600 (Penard); i, Amphitrema flavum, X360 (Cash and Wailes); j, Pseudodifflugia gracilis, X330 (Cash); k, Diaphoropodon mobile, X270 (Cash and Wailes); 1, m, Clypeolina marginata, X330 (Cash and Wailes).

grains

Genus Phryganella Penard. Test spheroidal or ovoid, with sandand minute diatom shells; aperture terminal, round; pseudopodia drawn out to a point; fresh water. P. acropodia (Hertwig and Lesser) (Fig. 205, c). Test circular in

486

PROTOZOOLOGY
view; hemispherical in profile; yellowish or brownish,

aperture

semi-transparent, and covered with sand-grains and scales; in front

view sharply pointed pseudopodia radiating; colorless endoplasm usually with chlorophyllous bodies; 30-50/i in diameter. Genus Bullinula Penard. Test ellipsoidal, flattened on one face, with silicious plates; on the flattened surface, -shaped aperture; a single nucleus; pseudopodia digitate or spatulate, simple or branched; fresh water. B. indica P. (Fig. 205, d). Test dark brown; 120-250/z in diameter. Distribution and morphology (Hoogenraad, 1933). Genus Heleopera Leidy. Test variously colored; fundus hemispherical, with sand-grains; surface covered with amorphous scales, often overlapping; aperture truncate, narrow, elliptic notched in narrow lateral view; a single nucleus; pseudopodia variable in number, thin digitate or branching; fresh water. Several species. H. petricola L. (Fig. 205, e, /). Test variable in size and color, strongly compressed; fundus rough with sand-grains of various sizes; aperture linear or elliptic, convex in front view; pseudopodia slender, branching; 80-lOOju long; in boggy places. Genus Averintzia Schouteden. Test similar to that of Heleopera, but small aperture elliptical; test thickened around aperture; fresh
water.

A. cyclostoma (Penard). Test dark violet, with sand-grains of

dif-

ferent sizes; elliptical in cross-section; pseudopodia unobserved; 135-

180^ long; in sphagnum and aquatic plants. Genus Nadinella Penard. Test chitinous, thin, hyaline, with foreign bodies and collar around aperture; filo podia; fresh water.

N.

tenella P. (Fig. 205, g).

50-55/x long; fresh water lakes.

Genus Frenzelina Penard. Two envelopes, outer envelope hemispherical, thin, rigid, covered with siliceous particles; inner envelope

round or ovoid, drawn out at aperture, thin, hyaline and covering the body closely; aperture round, through which a part of body with its often branching straight filo pods extends; cytoplasm with diatoms, etc.; a nucleus and a contractile vacuole; fresh water. F. reniformis P. (Fig. 205, h). Outer envelope 26-30/x in diameter; fresh water lakes.

Genus Amphitrema Archer. Test ovoid, symmetrical, compressed; composed of a transparent membrane, with or without adherent
foreign bodies; 2 apertures at opposite poles; with zoochlorellae;

nucleus central;

to several contractile vacuoles; straight

filo podia,

sparsely branched, radiating; fresh water. Several species.

A. flavum A. (Fig. 205,

i).

Test brown, cylindrical with equally

TESTACEA
rounded ends
in front view; elliptical in profile;

487

ovoid with a small

central oval aperture in end view; 45-77/*

sphagnum. Genus Pseudodifflugia Schlumberger. Test ovoid, usually rigid,

by

23-45/*; in

with foreign bodies; circular or elliptical in cross-section; aperture terminal; granulated cytoplasm colorless or greyish; nucleus posterior; a contractile vacuole; filo podia long, straight or branching; fresh
water. Several species.
S. (Fig. 205, j). Test yellowish or brownish; subspheriwith sand-grains; aperture without neck; 20-65/* long. Genus Diaphoropodon Archer. Test ovoid, flexible, with minute

P. gracilis

cal,

and a thick covering of hyaline hair-like projections; pseudopodia long, filose, branching; fresh water. D. mobile A. (Fig. 205, k). Test brown; of various shapes; aperture terminal; body does not fill the test; nucleus large; 1-2 contractile
foreign bodies

vacuoles; 60-120/* long; projections 8-10/* long; in vegetation.

Genus Clypeolina Penard. Test ovoid, compressed, formed of a double envelope; outer envelope composed of 2 valves with scales and particles; inner envelope a membranous sack; long filo podia,
often branching; fresh water.
C. marginata P. (Fig. 205, I, m). Outer test-valves }^ellow to dark brown; lenticular in cross-section; wide terminal aperture; endoplasm with many small globules; a single nucleus and contractile

vacuole; 80-150/* long.

Family 4 Euglyphidae Wallich

Genus Euglypha Dujardin (Pareuglypha Penard). Test hyaline, ovoid, composed of circular, oval, or scutiform siliceous imbricated
scales,

arranged in longitudinal rows; aperture bordered with reguarranged denticulate scales; usually with spines; 1-2 nuclei large, placed centrally; filopodia dichotomously branched; contraclarly

tile

vacuoles; fresh water.

(Ivanic, 1934).

Numerous

species. Division

and encyst-

ment

E. acanthophora (Ehrenberg) (E. alveolata D.) (Fig. 74). Test ovoid, or slightly elongate; 3-7 scales protruding around the circular
aperture; scales elliptical;

body almost
a).

fills

the test; 50-100/* long.

Test small, elongate with a long neck, fundus with 3-8 spines; scales oval; aperture circular, bordered by a single row of 5-6 denticulate scales; cytoplasm colorless; nucleus
E. cristata Leidy (Fig. 206,
posterior; reserve scales are said to
of aperture, unlike other species in

be collected around the exterior which they are kept within the

cytoplasm; 30-70/* long; 12-23/* in diameter; aperture 6-12/*; scales

4.5-9.5/*

by

2.5-6.5/*; spines 10-15/* long.

488

PROTOZOOLOGY

E. mucronata L. (Fig. 206, b). Test large; fundus conical, with 1-2 terminal spines (12-44^ long); aperture circular, bordered by a single row of 6-8 denticulate scales; 100-150^ long, diameter 30-60^; aperture 15-20ju in diameter.

Fig. 206. a, Euglypha cristata, X330 (Wailes); b, E. mucronata, X330 (Wailes); c, Paulinella chromatophora, X1000 (Wailes); d, Cyphoderia ampulla, X200 (Cash); e, f, Corythion pulchellum, X350 (Wailes).

Genus Paulinella Lauterborn. Test small ovoid, not compressed; with siliceous scales in alternating transverse rows; aperture terminal body does not fill the test completely nucleus posterior; among vegetation in fresh or brackish water. P. chromatophora L. (Fig. 206, c). Scales arranged in 11-12 rows; with 1-2 curved algal symbionts; no food particles; a single con;
;

tractile vacuole; 20-32ju long;

14-23^ in diameter.

Genus Cyphoderia Schlumberger. Test retort-shaped; colorless to yellow; made up of a thin chitinous membrane, covered with discs or scales; aperture terminal, oblique, circular; body does not fill the
test completely; nucleus large, posterior;
filose,

pseudo podia, few, long

simple or branched; fresh water (Husnot, 1943).

C. ampulla (Ehrenberg) (Fig. 206, d). Test usually yellow, translucent,

composed

of discs, arranged in diagonal rows; circular in

TESTACEA
cross-section; aperture circular; cytoplasm gray, with

489

many

granules

and food

particles; 2 contractile vacuoles; 60-200/* long; diameter

30-70/*. Several varieties.

Genus Trinema Dujardin. Test

small, hyaline, ovoid, compressed

anteriorly, with circular siliceous scales; aperture circular, oblique,

invaginate; nucleus posterior; filopodia not branched; fresh water in

vegetation.
T. enchelys (Ehrenberg) (Fig. 207, a). 1-2 contractile vacuoles;

Fig. 207. a, Trinema enchelys, X330 (Wailes); b, Placocista spinosa, X200 (Wailes); c, Assulina seminulum, X400 (Wailes); d, Nebela collaris, X200 (Cash); e, Quadrula symmetrica, X200 (Gash); f, Sphenoderia lenta, X330 (Leidy).

pseudo podia attenuate, radiating; 30-100/z long; 15-60/x wide; scales

4-12/x in diameter. T. lineare

Penard

(Fig. 79).

about

35/x

by

17/t; filopodia.

Test transparent; scales indistinct; Sexual fusion (Dunkerly, 1923) (p. 183).

Genus Corythion Taranek. Test small, hyaline, composed of small oval siliceous plates; compressed; elliptical in cross-section; aperture
subterminal, ventral or oblique, and circular or oval; numerous
filopodia; fresh water.

C. pulchellum

Penard

(Fig. 206,

e,

/).

Aperture lenticular; cyto-

plasm

colorless; 2-3 contractile vacuoles; 25-35/z

by

15-20/z; aper-

ture 7-1 0/x

by

3-4/x.

Genus Placocista Leidy. Test ovoid,

hyaline, compressed;

len-

ticular in cross-section; with oval or subcircular siliceous scales;

aperture wide, linear, with flexible undulate borders; nucleus large,

490

PROTOZOOLOGY
filo podia

posterior; often with zoochlorellae;

branching and man}',

generally arising from a protruded

portion of cytoplasm; fresh

spines,

water.

P. spinosa (Carter) (Fig. 207,

either singly or in pairs; 116-174/z

b). Margin of test with by 70-100^; in sphagnum.

colorless or brown; ovoid; with arranged in diagonal rows; aperture oval, terminal bordered by a thin chitinous dentate membrane; nucleus posterior;
elliptical scales,

Genus Assulina Ehrenberg. Test

contractile vacuoles;

filo podia

divergent, sometimes branching; fresh

water.

Body does not fill the test; with pseudo podia few, straight, divergent, slender, seldom branched; 60-150/x by 50-75^; in sphagnum. Genus Nebela Leidy. Test thin, ovate or pyriform; with circular or oval platelets of uniform or various sizes; highly irregular; endoplasm with oil globules; nucleus posterior; body does not fill the test, and is connected with the latter by many ectoplasmic strands at fundus end; pseudo podia blunt, rarely branched; fresh water.
A. seminulum numerous food
(E.) (Fig. 207, c).

particles;

Numerous species. Taxonomy

N.
collaris

(Jung, 1942a).

(Ehrenberg) (Fig. 207, d). Test pyriform, fundus obtuse in profile; aperture without any notch; endoplasm with chlorophyllous food particles; pseudopodia digitate, short, usually 3-6 in number: about 130m

by

85-90/*: in marshes

habit, binary fission

among sphagnum. Feeding and plasmogamy (MacKinlay, 1936).

dis-

Genus Quadrula Schulze. Test pyriform, hemispherical, or

coidal; with

quadrangular siliceous or calcareous platelets, arranged generally in oblique series, not overlapping; a single nucleus; body and pseudopodia similar to those of Difflugia; fresh water. Q. symmetrica (Wallich) (Fig. 207, e). Compressed, smaller platelets near aperture; cytoplasm very clear, with chlorophyllous granules; 3-5 pseudopodia digitate; nucleus posterior; 80-140/z by 40-

sphagnum. Genus Sphenoderia Schlumberger. Test globular or oval, sometimes slightly compressed; hyaline, membranous, with a short broad neck, and a wide elliptical aperture; scales circular, oval, or hexag96/*; in

onal, arranged in alternating series; cytoplasm colorless; 1-2 contractile vacuoles; filo podia, fine,

branching; fresh water.

test

S. lenta S. (Fig. 207, /).

Hyaline

ovoid or globular; scales

cir-

cular or broadly oval; aperture terminal, surrounded

colorless; 2 contractile vacuoles; 30-64/*

by a thin

chi-

tinous collar, one side inclined inwards; nucleus large; cytoplasm

by

20-46/*; aperture 10-22/*

in diameter.

TESTACEA
References

491

Belar, K.: (1921) Untersuchungen ueber Thecamoeben der Chlamydophrys-Gmppe. Arch. Protist., 43:287. Breuer, R. (1916) Fortpflanzung und biologische Erscheinungen einer Chlamydophrys-Form auf Agarkulturen. Ibid., 37:65. Cash, J.: (1905) The British freshwater Rhizopoda and Heliozoa. 1.
:

(1909)

2.

and Wailes, G. H.: (1915)

3.

(1918) 4. Deflandre, G.: (1928) Le genre Arcella. Arch. Protist., 64:152. (1929) Le genre Centropyxis. Ibid., 67:322. Dunkerly, J. S.: (1923) Encystation and reserve food formation in Trinema lineare. Tr. Roy. Soc. Edinburgh, 53:297. Foyn, B.: (1936) Ueber die Kernverhaltnisse der Foraminifere

Myxotheca arelilega. Arch. Protist., 87:272. Goette, A.: (1916) Ueber die Lebenscyclus von
Ibid., 37:93.

Difflugia lobostoma.

Hegner, R. W.:

(1920) The relation between nuclear number, chromatin mass, etc. J. Exper. Zool., 30: 1. Hoogenraad, H. R. (1933) Einige Beobachtungen an Bullinula
:

indica. Arch. Protist., 79:119. (1935) Studien ueber die sphagnicolen niederlandischen Fauna. Ibid., 84:1.

Rhizopoden der

(1936) Was ist Pamphagus mutabilis Bailey? Ibid., 87:417. P. (1943) Contribution a l'etude des Rhizopodes de Bretagne. Les Cyphoderia, etc. 143 pp. Paris. Ivanic, M.: (1934) Ueber die gewohnliche Zweiteilung, multiple

Husnot,

Teilung und Encystierung bei zwei Euglypha-Arten. Arch.

Protist., 82:363.

(1916) Heredity, variation and the results of sereproduction of Difflugia corona. Genetics, 1:407. (1937) Formation, inheritance and variation of the teeth in Difflugia corona. J. Exper. Zool., 77:287. Jepps, Margaret W. (1934) On Kibisidytes marinus, etc. Quart. J. Micr. Sc, 77:121. Jollos, V.: (1924) Untersuchungen ueber Variabilitat und Vererbung bei Arcellen. Arch. Protist., 49:307. Jung, W.: (1942) Sudchilenische Thekamoeben. Ibid., 95:253.

Jennings, H.

S.:

lection in the uniparental

(1942a) Illustrierte Thekamoeben-Bestimmungstabellen.

Ibid., 95:357.

I.

Leidy, U.
J.

(1879) Freshwater Rhizopods of North America. Rep. Surv. Terr., 12. MacKinlay, Rose B.: (1936) Observations on Nebela collaris, etc.
J.:

S. Geol.

Roy. Micr. Soc, 56:307.

:

Penard, E. (1890) Etudes sur

les rhizopods d'eau douce. Mem. soc. phys. hist, nat., Geneva, 31:1. (1902) Faune rhizopodique du bassin du Leman. Geneva. (1905) Sarcodines des Grands Lacs. Geneva.

492

PROTOZOOLOGY

Stump, A. B.: (1943) Mitosis and cell division in Pontigulasia vas. J. El. Mitch. Sc. Soc, 59:14. Valkanov, A.: (1930) Morphologie und Karyologie cer Microgromia elegantula. Arch. Protist., 71:241. (1931) Beitrag zur Morphologie und Karyologie der MicroVolz,
cometes paludosa. Ibid., 73:367. P.: (1929) Studien zur Biologie

der bodenbewohnenden

Thekamoeben.

Ibid.,

69:348.

Chapter

21

Order 5 Foraminifera d'Orbigny

Foraminifera THE most
logic times
(p. 10).

are comparatively large Protozoa, living

al-

exclusively in the sea.

They were very abundant

in geo-

forms are important in applied geology on ocean bottom, moving about sluggishly over the mud and ooze by means of their pseudopodia. Some are attached to various objects on the ocean floor, while others are

and the

fossil

The majority

live

pelagic.

The cytoplasm is ordinarily not differentiated into the two zones and streams out through the apertures, and in perforated forms through the numerous pores, of the shell, forming rhizopodia which are fine and often very long and which anastomose with one another to present a characteristic appearance (Fig. 5). The streaming movement of the cytoplasm in the pseudopodia are quite striking; the granules move toward the end of a pseudopodium and stream back along its periphery. The body cytoplasm is often loaded with brown granules which are apparently waste matter and in some forms such as Peneroplis pertusus these masses are extruded from the body from time to time, especially prior to the formation of a new chamber. Contractile vacuoles are usually not

found in the Foraminifera. form and structure. orange, red, brown, etc. The maIt may show various colorations jority measure less than one millimeter, although larger forms may frequently reach several millimeters. The test may be siliceous or calcareous and in some forms, various foreign materials, such as sand-grains, sponge-spicules, etc. which are more or less abundantly found where these organisms live, are loosely or compactly cemented together by pseudochitinous or gelatinous substances. Certain forms show a specific tendency in the selection of foreign materials for the test (p. 47). Siliceous tests are comparatively rare, being found in some species of Miliolidae inhabiting either the brackish water or deep sea. Calcareous tests are sometimes imperforated, but even in such cases those of the young are always perforated. By far the majority of the Foraminifera possess perforated calcareous tests. The thickness of the shell varies considerably, as do also the size and number of apertures, among different species. Frequently the perforations are very small in the young and later become large and coarse, while in others the reverse may be the case. The form of the shell varies greatly. In some there is only one chamber composed of a central body and radiating arms which repre-

The

test of the Foraminifera varies greatly in

493

494

PROTOZOOLOGY
Rhabdam209, a) or of a tubular
,

sent the material collected around the pseudopodia, as in

mina (Fig.
209, d).

body alone, as in Hyperammina (Fig.

possess shells of various spirals.

The polythalamous forms

chamber
is

which may be formed two swarmers or by asexual reproduction. The former is ordinarily small and known as the microspheric proloculum, while the latter, which is usually large, is called the megalospheric proloculum. To the proloculum are added many chambers which may be closely or loosely coiled or not coiled at all. These chambers are ordinarily undivided, but in many higher forms they are divided into chamberlets. The chambers are delimited by the suture on the exterior of the shell. The septa which divide the chambers are perforated by one or more foramina known as stolon canals, through which the protoplasm extends throughout the chambers. The last chamber has one or more apertures of variable sizes, through which the cytoplasm extends to the exterior as pseudopodia. The food of Foraminifera consists mostly of diatoms and algae, though pelagic forms are known to capture other Protozoa and micro crustaceans.

The

first

called the proloculum.

either

by the union

of

All species of Foraminifera manifest a

more or

less distinct

tend-

ency toward a dimorphism: the megalospheric form has a large proloculum, is uninucleate and is relatively small in size while the microspheric form possesses a small proloculum, is multinucleate, and is
;

large. In addition, there is a difference in the direction of rotation of

spiral

chambers of

tests in

some

species (Myers).

For example,

in

Discorbis opercularis, the microspheric form has clockwise rotation

of the chambers,

wise rotation.

The megalospheric forms

and the megalospheric form shows counterclockare said to be much more

numerous than the microspheric forms, especially in pelagic species. It is possible that, as Myers (1938) pointed out, the flagellate gametes are set free in open water and have a minimum of opportunity for syngamy. Lister (1895) observed the development of the megalospheric form in Elphidium by asexual reproduction from the microspheric form. He noticed flagellated swarmers in megalospheric tests and considered them as gametes which through syngamy gave rise to microspheric individuals. Recent studies by Myers (1935-1940) confirm the correctness of this view, except that in some species the
gametes are amoeboid. In Spirillina vivipara (Fig. 208, A, 1-5) the mature microspheric form (1) which measures 125-1 52ju in diameter, becomes surrounded by an envelope composed of substrate debris and viscous substance. Within the "multiple fission cyst," nuclear and cytoplasmic fissions form numerous small uninucleate megalo-

FORAMINIFERA
spheric individuals which produce tests
(Si).

495

They grow

60-72/x in

and emerge from the cyst mature megalospheric forms which measure diameter. Two to four such individuals become associated
into

<

Spirilhna Fig. 208. Developmental cycles of Foraminifera (Myers). A, microsphere vim-para; B, Discorbis patelliformis; G. Elphidium crispa. 1, megaloforms; 2, megalospheric forms, a-c, enlarged views of young

and zygote spheric forms; 3, beginning of sexual reproduction; 4, gamete views formation, a-c, gametes; 5, young microsphere forms, a-c, enlarged
of

one in each species.

496

PROTOZOOLOGY
"fertilization cyst." (S).

and transform into

The nucleus

in each

individual divides twice or occasionally three times and thus formed

multinucleate bodies escape from the tests within the cyst envelope where many gametocytes are produced by multiple fissions. Each gametocyte which contains 12 chromosomes divides into two amoeboid haploid gametes by meiosis. Gametes developed from different parents presumably undergo fusion in pairs and zygotes are produced (4)- Each zygote becomes proloculum in which the nucleus divides twice and when the coiled tubular chamber of test grows to about three-quarters of a whorl, young microspheric individuals escape from the cyst and lead' independent existence (5) Myers reports the development of Patellina corrugata is similar to that of Spirillina, except the amoeboid gametes possess 12 haploid number of chromosomes.
.

In Discorbis patelliformis (Fig. 208, B, 1-5), the same investigator

noticed no fertilization cyst during the sexual reproduction, but two

megalospheric individuals come in contact and flagellate gametes are

produced in them. The zygotes develop within the space formed by the dissolution of septa between chambefs and tests; the zygote nucleus divides repeatedly within each zygote and forms about 40 nuclei before a test is secreted. In Elphidium crispa (Fig. 208, C, 1-5), there is no direct association of megalospheric individuals during sexual reproduction. The flagellated gametes produced in each, are set free in the water and the fusion of the gametes depends entirely upon the chance meeting. In Patellina corrugata and Discorbis vilardeboanus, Calvez (1950) finds that the postzygotic divisions of the nucleus are mitotic and the trophozoite nucleus is diploid, but meiosis occurs in the trophozoite just before multiple division.

More than 300 genera of extinct and living Foraminifera are now known. Cushman distinguished 45 families. The present work follows Cushman in recognizing and differentiating 44 families, and lists one genus as an example for each, but places Gromia and allied genera in the order Testacea (p. 472). Taxonomy (Cushman, 1948); ecology (Phleger and Walton, 1950; Phleger and Parker, 1951); distribution (Post, 1951, Ming, 1952).
Test entirely or in part arenaceous Test single-chambered or rarely an irregular group of similar chambers loosely attached Test with a central chamber, 2 or more arms; fossil and recent.
. .

Family

Astrorhizidae

FORAMINIFERA
Genus Rhabdammina Sars
(Fig. 209, a)

497

Test without a central chamber, elongate, open at both ends; fossil Family 2 Rhizamminidae and recent

Genus Rhizammina Brady

(Fig. 209, b)

Test a chamber or rarely series of similar chambers loosely attached, with normally a single opening; fossil and recent

Family 3 Saccamminidae

Genus Saccammina Sars

chamber

(Fig. 209, c)

Test 2-chambered, a proloculum and long undivided tubular second

Fig. 209.
algaeformis,

a,

Rhabdammina abyssorum, X5

(Ktihn); b,

Rhizammina

fragment of, Xl4 (Cushman); c, Saccammina sphaerica, X8 (Rhumbler); d, Hyperammina subnodosa, x4 (Brady); e, Ammodiscus incertus, X20 (Kiihn); f, Silicina limitata, Xl3 (Cushman); g, Reophax nodulosus, X3 (Brady).
Test with the second chamber, simple or branching, not coiled; mostly recent and also fossil Family 4 Hyperamminidae

Genus Hyperammina Brady

(Fig. 209, d)

Test with the second chamber usually coiled at least in young Test of arenaceous material with much cement, usually yellowish or reddish brown; fossil and recent Family 5 Ammodiscidae
.

Genus Ammodiscus Reuss

(Fig. 209, e)

Test of siliceous material, second chamber partially divided; fossils only Family 6 Silicinidae

Genus

Silicina

Bornemann

(Fig. 209, f)

Test typically many-chambered Test with all chambers in a rectilinear series;

fossil

and recent Family 7 Reophacidae

498

PROTOZOOLOGY
Genus Reophax Montfort
(Fig. 209, g)

Test planispirally coiled at least in young Axis of coil, short; many uncoiled forms;

fossil

and recent Family 8 Lituolidae

Genus Lituola Lamarck

Axis of
coil

(Fig. 210, a)

usually long, all close-coiled Interior not labyrinthic; fossil only

Family

9 Fusulinidae

^Hs

Fig. 210. a, Lituola nautiloidea (Cushman); b, section through a Fusulina (Carpenter); c. Textularia agglutinans, X90 (Rhumbler); d. Verneuilina propinqua, XS (Brady); e, Valvulina triangularis, (d'Orbigny); f, Trochammina inflata, X32 (Brady); g, Placopsilina cenomana (Reuss); h, Tetrataxis palaeotrochus, Xl5 (Brady); i, Spiroloculina limbata, X20 (Brady); j, Triloculina trigonula, Xl5 (Brady) k, Fischerina helix, X32 (Heron-Allen and Earland); 1, Vertebralina striata, X40 (Kuhn); m, Alveolinella mello, X35 (Brady).
;

Genus Fusulina Fisher

Interior labyrinthic; fossil only

(Fig. 210, b)

Family 10 Loftusiidae

Genus Loftusia Brady

Test typically biserial at least in young of microspheric form; fossil and recent Family 11 Textulariidae

Genus Textularia Def ranee

(Fig. 210, c)

Test typically triserial at least in young of microspheric form Aperture usually without a tooth, test becoming simpler in higher forms; fossil and recent Family 12 Verneuilinidae

FORAMINIFERA
Genus Verneuilina d'Orbigny
(Fig. 210, d)

499

Aperture typically with a tooth, test becoming conical in higher Family 13 Valvulinidae forms; fossil and recent

Genus Valvulina d'Orbigny

(Fig. 210, e)

Test with whole body labyrinthic, large, flattened, or cylindrical; Family 14 Neusinidae recent

Genus Neusina Goes

Test trochoid at least while young

Mostly

free, typically trochoid

throughout;

fossil and recent. Family 15 Trochamminidae

.

Genus Trochammina Parker and Jones

recent

(Fig. 210,/)

Attached; young trochoid, later stages variously formed;

fossil and Family 16 Placopsilinidae

Genus Placopsilina d'Orbigny

(Fig. 210, g)

Free; conical, mostly of large size; fossil only

Family 17 Orbitolinidae

Genus Tetrataxis Ehrenberg

(Fig. 210, h)

Test coiled in varying planes, wall imperforate, with arenaceous portion only on the exterior; fossil and recent

Family 18 Miliolidae

(in part)

Genus Spiroloculina d'Orbigny

(Fig. 210,

i)

Test calcareous, imperforate, porcellaneous Test with chambers coiled in varying planes, at least in young; aperture large, toothed; fossil and recent. .Family 18 Miliolidae (in part)

Genus Triloculina d'Orbigny

Test trochoid;
fossil

(Fig. 210, j)

and recent

Family 19 Fischerinidae
(Fig. 210, k)

Genus Fischerina Terquem

Test planispiral at least in young Axis very short, chambers usually simple;

fossil and recent Family 20 Ophthalmidiidae

Genus Vertebralina d'Orbigny

(Fig. 210,

I)

Axis short, test typically compressed and often discoid, chambers mostly with many chamberlets; fossil and recent Family 21 Peneroplidae

Genus Peneroplis Montfort

(Figs. 4; 211)

Axis typically elongate, chamberlets developed; mainly fossil Family 22 Alveolinellidae

500

PROTOZOOLOGY

i/w

|V

&

^6

ft

c,

toc

Fig. 211. Diagram illustrating the life-cycle of Peneroplis pertusus (Winter), a-f, megalospheric generation; g, gamete formation; h-k, isogamy; 1-n, microspheric generation; o, multiple division.

Genus

Alveolinella Douville (Fig. 210,

w)

Test globular, aperture small, not toothed; recent only Family 23 Keramosphaeridae

Genus Keramosphaera Brady

Test calcareous, perforate Test vitreous with a glassy
trochoid
lustre,

aperture typically radiate, not

FORAMINIFERA

501

Test planispirally coiled or becoming straight, or single-chambered; fossil and recent Family 24 Lagenidae

Genus Lagena Walker and Jacob

Test biserial or elongate spiral;
fossil

(Fig. 212, a)

and recent Family 25 Polymorphinidae

Genus Polymorphina d'Orbigny

Test not vitreous; aperture not radiating Test planispiral, occasionally trochoid, then usually with processes along the suture lines, septa single, no canal system; fossil and recent Family 26 Nonionidae

Fig. 212. a, Lagena striata, X50 (Rhumbler); b, Elphidium strigilata, (Kiihn); c, Operculina ammonoides, X50 (Kuhn); d, Pavonina flabelliformis, X30 (Brady); e, Hantkenina alabamensis, X40 (Cushman); f, Bolivina -punctata, X100 (Kuhn); g, Rotalia beccarii, X40 (Kiihn); h, Asterigerina carinata, X30 (d'Orbigny from Kiihn).

X40

Genus Elphidium Montfort

(Figs. 5; 208,

C; 212,

b)

(Polystomella Lamarck)

Test planispiral, at least in young, generally lenticular, septa double, canal system in higher forms; fossil and recent Family 27 Camerinidae

Genus Operculina d'Orbigny

(Fig. 212, c)

Test generally biserial in at least microspheric form, aperture usually large, without teeth; fossil and recent Family 28 Heterohelicidae

502

PROTOZOOLOGY
Genus Pavonina d'Orbigny
Test planispiral,
bi-

(Fig. 212, d)

or tri-serial with elongate spines and lobed aperture; fossil and recent Family 29 Hantkeninidae

Genus Hantkenina Cushman

(Fig. 212, e)

Test typically with an internal tube, elongate Aperture generally loop-shaped or cribrate;
.

fossil and recent. Family 30 Buliminidae

.

Genus Bolivina d'Orbigny

fossil, also

(Fig. 212, /)

Aperture narrow, curved, with an overhanging portion; mostly

recent

Family 31 Ellipsoidinidae

Genus

Ellipsoidina Seguenza

Test trochoid, at least in young of microspheric form, usually coarsely perforate; when lenticular, with equatorial and lateral chambers Test trochoid throughout, simple; aperture ventral

No

alternating supplementary chambers on ventral side; fossil and recent Family 32 Rotaliidae

Genus Rotalia Lamarck

(Fig. 212, g)
(Fig. 208,

Genus

Spirillina

Ehrenberg

A)

Genus Patellina Williamson. Genus Discorbis Lamarck

(Fig. 208,

B)

Alternating supplementary chambers on ventral side; fossil and recent Family 33 Amphisteginidae

Genus Asterigerina d'Orbigny

With supplementary material and chambers; fossil and recent

(Fig. 212, h)

Test trochoid and aperture ventral in young

large spines, independent of

Family 34 Calcarinidae
(Fig. 213, a)

Genus Calcarina d'Orbigny

With
later

chambers in annular series or globose with multiple apertures, but not covering earlier ones; fossil and recent. Family 35 Halkyardiidae
. . .

Genus Halkyardia Heron-Allen and Earland

With
later

(Fig. 213, b)

chambers somewhat biserial; aperture elongate in the axis of coil; fossil and recent. .Family 36 Cassidulinidae

FORAMINIFERA
Genus Cassidulina d'Orbigny
With
later

503

(Fig. 213, c)

chambers becoming involute, very few making up the

exterior in adult; aperture typically elongate, semicircular; in a few species circular; fossil and recent Family 37 Chilostomellidae

Genus Allomorphina Reuss

With chambers mostly
for pelagic
life,

(Fig. 213, d)

and wall cancellated, adapted, globular forms with the last chamber completely involute; aperture umbilicate or along the suture; fossil and recent Family 38 Globigerinidae
finely spinose

Fig. 213. a, Calcarina defrancei, X25 (Brady); b, Halkyardia radiata, Xl5 (Cushman); c, Cassidulina laevigata, X25 (Brady); d, Allomorphina trigona, X40 (Brady); e, Globigerina bxdloides, X30 (Kuhn); f, Anomalina punctulata (d'Orbigny); g, Rupertia stabilis, X50 (Brady).

Genus Globigerina d'Orbigny

(Fig. 213, e)

Early chambers globigerine, later ones spreading and compressed; fossil and recent Family 39 Globorotaliidae

Genus Globorotalia Cushman

Test trochoid at least in young, aperture peripheral or becoming
dorsal

Mostly attached, dorsal side usually flattened; fossil and recent Family 40 Anomalinidae

Genus Anomalina d'Orbigny

Later chambers in annular series;
fossil

(Fig. 213, /)

and recent Family 41 Planorbulinidae

504

PROTOZOOLOGY
Genus Planorbulina d'Orbigny
Test trochoid in very young, later growing upward Later chambers in loose spiral; fossil and recent

Family 42 Rupertiidae

Genus Rupertia Wallich

(Fig. 213, g)

Later chambers in masses or branching, highly colored; mostly Family 43 Homotremidae recent, also fossil

Genus Homotrema Hickson

Test trochoid in the very young of microspheric form, chambers becoming annular later, with definite equatorial and lateral chambers, often with pillars; fossil only Family 44 Orbitoididae

Genus Orbitoides d'Orbigny

References

Brady, B. H.: (1884) Report on the Foraminifera dredged by H.M.S. Challenger, during the years 1873-1876. Rep. Voy.
Chall., 9.

Calvez,

le: (1950) Recherches sur les foraminiferes. II. Arch. 87:211. Cushman, J. A.: (1948) Foraminifera: their classification and economic use. 4 ed. Cambridge, Mass. Illing, Margaret A.: (1952) Distribution of certain Foraminifera within the littoral zone on the Bahama Banks. Ann. Mag. Nat. Hist., 5:275. Myers, E. H.: (1935) The life history of Patellina corrugata, etc. Bull. Scripps Inst. Oceanogr., Univ. California Tech. Ser., 3: 355. (1936) The life-cycle of Spirillina vivipara Ehrenberg, with notes on morphogenesis, etc. J. Roy. Micr. Soc, 56:126. (1938) The present state of our knowledge concerning the life cycle of the Foraminifera. Proc. Nat. Acad. Sc, 24:10. (1940) Observations on the origin and fate of flagellated gametes in multiple tests of Discorbis. J. Mar. Biol. Ass. Unit. Kingd., 24:201. Phleger, F. B.: (1951) Ecology of Foraminifera, northwest Gulf of Mexico. I. Mem. Geol. Soc. America, 46:1. and Parker, F. L.: (1951) II. Ibid., 46:89. and Walton, W. R.: (1950) Ecology of marsh and bay Foraminifera, Barnstable, Mass. Am. J. Sc, 248:274. Post, Rita J.: (1951) Foraminifera of the south Texas coast. Publ. Inst. Mar. Sc, 2:165. Rhumbler, L.: (1904) Systematische Zusammenstellung derrezenten Reticulosa (Nuda u. Foraminifera). I. Arch. Protist., 3: 181.
J.

zool. exper. gn.,

Chapter 22
Subclass 2 Actinopoda Calkins
Actinopoda are divided THE Without
central capsule

into

two orders as follows:

Order 1 Heliozoa Order 2 Radiolaria (p. 516)

With central capsule

Order

Heliozoa Haeckel

a rule, spherical in form with many radiating axopodia. The cytoplasm is differentiated, distinctly in Actinosphaerium, or indistinctly in other species, into the coarsely vacuolated ectoplasm and the less transparent and vacuolated endoplasm. The food of Heliozoa consists of living Protozoa or

The Heliozoa

are, as

Protophyta; thus their mode of obtaining nourishment

is

holozoic.

A large organism may sometimes be captured by a group of Heliozoa

which gather around the prey. When an active ciliate or a small rotifer comes in contact with an axopodium, it seems to become suddenly paralyzed and, therefore, it has been suggested that the pseudopodia
contain some poisonous substances.

The

axial filaments of the axo-

podia disappear and the pseudopodia become enlarged and surround the food completely. Then the food matter is carried into the main
part of the body and
contractile vacuoles
is

digested.

The ectoplasm

contains several

and numerous refractile granules which are scattered throughout. The endoplasm is denser and usually devoid of granules. In the axopodium, the cytoplasm undergoes streaming movements. The hyaline and homogeneous axial filament runs straight through both the ectoplasm and the endoplasm, and terminates in a point just outside the nuclear membrane. When the pseudopodium is withdrawn, its axial filament disappears completely, though the latter sometimes disappears without the withdrawal of the pseudopodium itself. In Acanthocystis the nucleus is eccentric (Fig. 216, b), but there is a central granule, or centroplast, in the center of the body from which radiate the axial filaments of
the axopodia. In multinucleate Actinosphaerium, the axilia filaments
axial filament arises

terminate at the periphery of the endoplasm. In Camptonema, an from each of the nuclei (Fig. 214, d).

The
species.

skeletal structure of the Heliozoa varies

among

different

The body may be naked, covered by a

gelatinous mantle, or

provided with a lattice-test with or without spicules. The spicules are variable in form and location and may be used for specific differentiation. In some forms there occur colored bodies bearing

chromatophores, which are considered as holophytic Mastigophora

505

506
(p.

PROTOZOOLOGY
29) living in the heliozoans as symbionts.
fission or

The Heliozoa multiply by binary

division

budding. Incomplete

may

result in the formation of colonies, as in Rhaphidi-

ophrys. In Actinosphaerium, nuclear

phenomena have been studied

and Oxnerella behaves somewhat like the centriole in a metazoan mitosis. Budding has been known in numerous species. In Acanthocystis the nucleus undergoes amitosis several times, thus forming several nuclei, one of which remains in place while the other migrates toward the body surface. Each peripheral nucleus becomes surrounded by a protruding cytoplasmic body which becomes covered by spicules and which is set free in the water as a bud. These small individuals are supposed to grow into larger forms, the central granules being produced from the nucleus during the growth. Formation of swarmers is known in a few genera and sexual reproduction occurs in some forms. The Heliozoa live chiefly in fresh water, although some inhabit the sea. Taxonomy and morphology (Penard, 1905, 1905a; Cash and Wailes, 1921; Roskin, 1929, Valkanov, 1940).

by

several investigators (p. 204). In Acanthocystis

(Fig. 59), the central granule

Without gelatinuous envelope Without flagella Pseudopodia arise from thick basal

parts,

branching

Family 1 Actinocomidae Pseudopodia not branching, cytoplasm highly vacuolated Family 2 Actinophryidae (p. 507) Family 3 Ciliophryidae (p. 508) With 1-2 flagella

With gelatinous envelope; with or without skeleton Without flagella Without chitinous capsule Family 4 Lithocollidae Without definite skeleton With chitinous or siliceous spicules or scales .Family 5 Heterophryidae With chitinous spicules. With siliceous skeleton
. .

(p.

508)

(p.

510)

Cup-like plates over body; 2-3 pseudopodia often grouped Family 6 Clathrellidae (p. 511) Scales flattened, not cup-like Family 7 Acanthocystidae (p. 511) Family 8 Clathulinidae (p. 513) With chitinous retiform capsule With numerous flagella, among axo podia; siliceous scales Family 9 Myriophryidae (p. 514)

Family

Actinocomidae Poche

Genus Actinocoma Penard. Body spherical; one or more contractile vacuoles; nucleus with a thick membrane, central; filopodia, not
axo podia, simple or in brush-like groups; fresh water. A. ramosa P. (Fig. 214, a). Average diameter 14-26ju.

ACTINOPODA, HELIOZOA
Family 2 Actinophyridae Claus

507

Genus Actinophrys Ehrenberg. Spheroidal; cytoplasm highly vacuolated, especially ectoplasm; with often symbiotic zoochlorellae;

nucleus central;

to

many

contractile vacuoles; axopodia straight,

Fig. 214.

a,

X400 (Kudo);

Actinocoma ramosa, X630 (Penard); b, Actinophrys sol, c, Actinosphaerium eichhorni, X45 (Kudo); d, Camp-

tonema nutans, X350 (Schaudinn).

numerous, axial filaments terminate at surface of the nucleus; "sun

animalcules"; fresh water.

A. sol E. (Figs. 90; 214, b). Spherical; ectoplasm vacuolated; endoplasm granulated with numerous small vacuoles; a large central nucleus; solitary but may be colonial when young; diameter variable, average being 40-50^; among plants in still fresh water. Reproduction, morphology and physiology (Belaf, 1923, 1924); food habit
(Looper, 1928).

508

PROTOZOOLOGY

A. vesiculata Penard. Ectoplasm with saccate secondary vesicles, extending out of body surface between axo podia; nucleus central, with many endosomes; 25-30/x in average diameter; fresh water. Genus Actinosphaerium Stein. Spherical; ectoplasm consists al-

most entirely of large vacuoles in one or several layers; endoplasm with numerous small vacuoles; numerous nuclei; axopodia end in
the inner zone of ectoplasm (Fig.
6).

2 species.

A. eichhorni Ehrenberg (Figs. 6; 214, c). Numerous nuclei scattered in the periphery of endoplasm; 2 or more contractile vacuoles, large; axial filaments arise from a narrow zone of dense cytoplasm at the border line between endoplasm and ectoplasm; body large, diameter 200-300/x, sometimes up to 1 mm.; nuclei 12-20^ in diameter; among
vegetation in freshwater bodies. Nuclear change (Speeth, 1919); morphology (Rumjantzew and Wermel, 1925); transplantation

(Okada, 1930). A. arachnoideum Penard. Ectoplasm irregularly vacuolated; no distinct endoplasmic differentiation; nuclei smaller in number; pseudopodia of 2 kinds; one straight, very long and the other filiform, and anastomosing; 70-80m in diameter; fresh water. Genus Camptonema Schaudinn. Spheroidal; axial filaments of

axopodia end

in nuclei

about 50 in number; vacuoles numerous and

small in size; salt water.

C. nutans S. (Fig. 214, d). About 150^ in diameter. Genus Oxnerella Dobell. Spherical; cytoplasm indistinctly differentiated eccentric nucleus with a large endosome axial filaments
;
;

take their origin in the central granule; no contractile vacuole;

nuclear division typical mitosis (Fig. 59). 0. maritima D. (Fig. 59). Small, 10-22/1 in diameter; solitary,
floating or creeping; salt water.

Family 3 Ciliophryidae Poche

Genus Ciliophrys Cienkowski. Spherical with extremely

fine

radiating filopodia, giving the appearance of a typical heliozoan,

with a single flagellum which is difficult to distinguish from the numerous filopodia, but which becomes conspicuous when the pseudopodia are withdrawn; fresh or salt water. C. infusionum C. (Fig. 215, a). 25-30^ long; freshwater infusion. C. marina Caullery. About 10^ in diameter; salt water.

Family 4 Lithocollidae Poche

Genus

Lithocolla Schulze. Spherical body; outer envelope with

;

usually one layer of sand-grains, diatoms, etc. nucleus eccentric.

ACTINOPODA, HELIOZOA
L. globosa S. (Fig. 215,
6).

509

Body

reddish with numerous small

colored granules; nucleus large; central granule

unknown; envelope

35-5(V
water.

in diameter; in lakes, ponds,

and

rivers; also in brackish

globosa,

Ciliophrys infusionum, X400 (Biitschli); b, Lithocolla Astrodisculus radians, X600 (Penard); c, d, Actinolophus pedunculatus, X400 (Schultze); e, Elaeorhanis cincta, X300 (Penard); f, Sphaerastrum fockei, X300 (Stubenrauch) g, HeteroFig. 215.
a,

X250 (Penard);

phrys myriopoda,

X270 (Penard).

510

PROTOZOOLOGY
Greeff. Spherical with gelatinous envelope,

Genus Astrodisculus
free

sometimes absent; no demarcation between 2 regions of the cytoplasm; pseudopodia fine without granules; fresh

from

inclusions,

water.
c). Outer surface usually with adherent and bacteria; cytoplasm often loaded with green, yellow, or brown granules; nucleus eccentric; a contractile vacuole; diameter 25-30/z including envelope; in pools and ditches.

A. radians G. (Fig. 215,

foreign bodies

Genus Actinolophus Schulze. Body pyriform, enveloped

numerous; nucleus eccentric;
A. pedunculatus
salt water.

in

gelatinous mantle; stalked; stalk apparently hollow; axopodia long,

S. (Fig. 215, d).

Diameter about

30yu; stalk

about

100m long. Genus Elaeorhanis Greeff. Spherical; mucilaginous envelope with sand-grains and diatoms; cytoplasm with a large oil globule; nucleus eccentric;
1

or

more

contractile vacuoles; pseudopodia not

granulated, sometimes forked; fresh water.

E. cincta G. (Fig. 215, e). Bluish with a large yellow oil globule; without any food particles; no central granule; pseudopodia rigid, but apparently without axial filaments, sometimes forked; young forms colonial; solitary when mature; outer diameter 50-60/z; body

25-30^; in lakes and pools. Genus Sphaerastrum Greeff. Somewhat flattened; greater part of axopodia and body covered by a thick gelatinous mantle; a central granule and an eccentric nucleus; fresh water. S. fockei G. (Fig. 215, /). Diameter about 30/x; often colonial; in swamps.
itself

Family 5 Heterophryidae Poche

thick, with

Genus Heterophrys Archer. Spherical; mucilaginous envelope numerous radial, chitinous spicules which project beyond

periphery; nucleus eccentric; axial filaments originate in a central

granule; fresh or salt water.

H. myriopoda A. (Fig. 215, g). Nucleus eccentric; cytoplasm loaded with spherical algae, living probably as symbionts; contractile vacuoles indistinct; 50-80/z in diameter; in pools and marshes; and
also

among marine algae. H. glabrescens Penard. Spherical; gelatinous envelope poorly developed; chitinous needles indistinct; pseudopodia very long; 11 15u
in

diameter; fresh water.

ACTINOPODA, HELIOZOA
Family 6 Clathrellidae Poche

oil

Genus Clathrella Penard. Envelope distinct, polygonal; surface with uniform alveoli with interalveolar portion extending out; envelope appears to be continuous, but in reality formed by a series of cup-like bodies; contractile vacuole large; voluminous nucleus
eccentric;
filo podia

straight,

some

bifurcated,

arising

between

"cups."
C. foreli P. (Fig. 21(3, a). fresh water.

Envelope about 40-55ju

in diameter;

Family

7 Acanthocystidae Claus

Genus Acanthocystis Carter. Spherical; siliceous scales, arranged tangentially and radiating siliceous spines with pointed or bifurcated ends; nucleus eccentric; a distinct central granule in which
the axial filaments terminate. Several species.

A. aculeata Hertwig and Lesser (Fig. 216,

ish;

b).

Tangential scales

stout and pointed; spines curved and nail-headed; cytoplasm grey-

a single contractile vacuole; diameter 35-40>; spines about 1/3 the body diameter; in fresh water. Morphology and reproduction
(Stern, 1924).

Genus Pompholyxophrys Archer. Spherical; outer mucilaginous envelope with minute colorless spherical granules arranged in concentric layers; nucleus eccentric; contractile vacuoles; pseudopodia
long, straight, acicular; fresh water.

P. punicea A. (Fig. 21G,

c).

Body

colorless or reddish, with usually

many

colored granules and green or

large, eccentric; solitary, active;

brown food particles; nucleus diameter 25-35^; outer envelope

5-10/x larger; in pools.

Genus Raphidiophrys Archer. Spherical; mucilaginous envelope with spindle-shaped or discoidal spicules which extend normally outwards along pseudopodia; nucleus and endoplasm eccentric;
solitary or colonial; fresh water. Several species.

R. pallida Schulze (Fig. 216, d). Outer gelatinous envelope crowded with curved lenticular spicules, forming accumulations around pseudopodia; ectoplasm granulated; nucleus eccentric; contractile vacuoles; axial filaments arise from the central granule;
solitary;

diameter 50-60>; nucleus 12-15^ in diameter; spicules 2G>

in
still

long;

among vegetation
found in the

fresh water.
of various forms, but un-

Genus Raphidocystis Penard. Spicules

like those

last genus.
e).

R. tubifera P. (Fig. 216,

Spicules tubular with enlarged extrem-

512
ity;

PROTOZOOLOGY
diameter about
18/x;

envelope 25^; fresh water. Body 20-40/* in diameter; thin axopodia twice the body diameter; without radial spicules; feeds on ciliates
R. infestans Wetzel.
(Wetzel, 1925).

Genus Wagnerella Mereschkowsky.

Spherical, supported

by a

X300

Fig. 216. a, Clathrella foreli, X250 (Penard); b, Acanthocystis aculeata, (Stern); c, Pompholyxophrys punicea, X260 (West); d, Raphidio-

phrys pallida, X300 (Penard); e, Raphidocyslis tubifera, X500 (Penard); f, Wagnerella borealis, X75 (Kuhn); g, Pinaciophora fltiviatilis, X250 (Penard).

ACTINOPODA, HELIOZOA
cylindrical stalk with

513
siliceous spicules;

an enlarged base; small

nucleus in the base of stalk; multiplication by budding.

W. borealis M. (Fig. 216, /). About I8O/1 in diameter; stalk often up to 1.1 mm. long; salt water. Genus Pinaciophora GreefT. Spherical; outer envelope composed of circular discs, each being perforated with 19 minute pores; cytoplasm reddish fresh water. P. fluviatilis G. (Fig. 216, g). Diameter 45-50ju, but somewhat
;

variable; in freshwater ponds.

Family 8 Clathrulinidae Claus

Genus Clathrulina Cienkowski. Envelope spherical, homogeneous, with numerous regularly arranged openings; with a stalk; protoplasm central, not filling the capsule; nucleus central; pseudo podia numerous, straight or forked, granulated fresh water.
;

C. elegans C. (Fig. 217, a).

Envelope

colorless to

brown, perforated

by numerous comparatively large circular or polygonal openings; 1 or more contractile vacuoles; nucleus central; diameter 60-90^,
openings 6-10m; length of stalk 2-4 times the diameter of envelope, 3-4 n wide; solitary or colonial; among vegetation in ponds. Taxon-

omy and

stalk formation (Valkanov, 1928).

Genus Hedriocystis Hertwig and Lesser. Envelope spherical, openings minute, surrounded by polyhedral facets or ridges; with
stalk; solitary or colonial; fresh water.

H.

reticulata

Penard
1

(Fig. 217, b).

Envelope

colorless or

pale

yellow, facets regularly polygonal with raised borders; stalk solid,

nucleus central;
25/* in

contractile vacuole; each

pesudopodium

arises

from a pore located

1.5/z; in

in the center of a facet; solitary; capsule

about

\2y. in diameter; stalk about 70// by marshy pools. Genus Elaster Grimm. Envelope spherical, delicate, penetrated by numerous more or less large pores; without stalk; pseudo podia many, straight filose. E. greeffi G. (Fig. 217, c). Diameter of envelope 20/*; envelope

diameter; body about

delicate, colorless;

many pseudopodia; in peaty soil.

Genus Choanocystis Penard. Spherical envelope with perforations

which possess conical borders; openings of cones provided with funnel-like expansions, edges of which nearly touch one another;
fresh water.
C. lepidula P. (Fig. 217, d).
1

Diameter 10-13^; envelope

delicate;

or more contractile vacuoles; pseudopodia very long.

514

PROTOZOOLOGY
Family 9 Myriophryidae Poche

protoplasmic envelope containing scales

Genus Myriophrys Penard. Spherical or ovoid, covered with a (?), surrounded by numer-

a, Clathrulina elegans, X250 (Leidy); b, Hedriocystis reticuX500 (Brown); c, Elaster greeffi,, X680 (Penard); d, Choanocystis lepidula, X690 (Penard); e, Myriophrys paradoxa, X300 (Penard).

Fig. 217.

lata,

ACTINOPODA, HELIOZOA
ous
fine processes;

515

large contractile vacuole; long pseudopodia granulated

endoplasm vesicular; a large nucleus eccentric; a and attenue).

ated toward ends.

M. paradoxa
swamps.

P. (Fig. 217,

Average diameter 4%;

in

fresh-water

References

Belar, K.: (1923) Untersuchungen an Actinophrys

Protist., 46:1.

sol.

I.

Arch.

(1924) II. Ibid., 48:371.

Cash, J. and Wailes, G. H.: (1921) The British freshwater Rhizopoda and Heliozoa. 5. London. Leidy, J.: (1879) Freshwater Rhizopods of North America. Rep.
U.
S. Geol.

Surv. Terr., 12.

Okada, Y. K.: (1930) Transplantationsversuche an Protozoen.

Penard, E.
Arch. Protist., 69:39. (1905) Les Heliozoaires d'eau douce. Geneva. (1905a) Les Sarcodines des grands lacs. Geneva. Roskin, G.: (1929) Neue Heliozoa-Arten. I. Arch. Protist., 66:201. Rumjantzew, A. and Wermel, E.: (1925) Untersuchungen ueber den Protoplasmabau von Aetinosphaerium eichhorni. Ibid., 52:
:

217.

Speeth, Caroline: (1919) Ueber Kernveranderungen bei Aetinosphaerium in Hunger- und Encystierungskulturen. Ibid., 40:
182.

Stern,

C:

(1924) Untersuchungen ueber Acanthocystideen. Ibid.,

48:437.

Valkanov,

A.: (1928) Protistenstudien. III. Ibid., 64:446. (1940) Die Heliozoen und Proteomyxien. Ibid., 93:225. Wetzel, A. (1925) Zur Morphologie und Biologie von Raphidocystis Ibid., 53 135. infestans n. sp., etc.
:

Chapter 23

Order 2 Radiolaria Miiller

made up chiefly have been equally abundant during former geologic ages, since rocks composed of their skeletons occur in various geological formations. Thus this group is the second group of Protozoa important to geologists.
floor is

Radiolaria are THE ocean known

pelagic in various oceans.

vast area of the

to be covered with the ooze

of radiolarian skeletons.

They seem

to

The body is generally spherical, although radially or bilaterally symmetrical forms are also encountered. The cytoplasm is divided distinctly into two regions which are sharply delimited by a membranous structure known as the central capsule. This is a single or double perforated membrane of pseudochitinous or mucinoid nature. Although its thickness varies a great deal, the capsule is ordinarily very thin and only made visible after addition of reagents. Its shape varies according to the form of the organism; thus in spherical forms it is spherical, in discoidal or lenticular forms it is more or less ellipsoidal, while in a few cases it shows a number of protruding processes. The capsule is capable of extension as the organism grows and of dissolution at the time of multiplication. The cytoplasm on either side of the capsule communicates with the other side through pores which may be large and few or small and numerous. The intracapsular portion of the body is the seat of reproduction, while the extracapsular region
is

nutritive
is

and hydrostatic

in function.

The

intrais

capsular cytoplasm

granulated, often greatly vacuolated, and

stratified either radially or concentrically. It contains

one or more

nuclei, pigments, oil droplets, fat globules,

is

and

crystals.

The nucleus

usually of vesicular type, but

different species

its

form,

size,

among

and

also at different

and structure, vary stages of development

even in one and the same species.

A thin assimilative layer, or matrix, surrounds the central capsule. In Tripylea, waste material forms a brownish mass known as phaeodium, around the chief aperture (astropyle) of the capsule. Then there is a highly alveolated region, termed calymma, in which the alveoli are apparently filled with a mucilaginous secretion of the cytoplasm. Brandt showed that the vertical movement of some Radiolaria is due to the formation and expulsion of a fluid which consists of water saturated with carbon dioxide. Under ordinary weather and temperature conditions, the interchange between the alveoli and the exterior is gradual and there is a balance of loss and gain of the fluid, so that the organisms float on the surface of the sea. Under
516

RADIOLARIA

517

rough weather conditions or at extraordinary high temperatures,

the pseudopodia are withdrawn, the alveoli burst, and the organisms descend into deeper water, where the alveoli are reformed.

The Radiolaria

feed

on microplankton such as copepods,

dia-

taken in through pseudopodia and passed down into the deeper region of calymma where it is digested in food vacuoles. The Radiolaria can, however, live under experimental conditions without solid food if kept under light.
toms, and various Protozoa.
is

The food

This is ordinarily attributed to the action of the yellow corpuscles which are present in various parts of the body, although they are, as a rule, located in the calymma. In Actipylea they are found only in intracapsular cytoplasm, and in Tripylea they are absent altogether. They are spherical bodies, about 15/x in diameter, with a cellulose wall, 2 chromatophores, a pyrenoid, starch, and a single nucleus. They appear to multiply by fission. These bodies are considered as zooxanthellae (p. 274). In the absence of organic food material, the Radiolaria live probably by utilizing the products of holo phytic nutrition of these symbiotic organisms. The axopodia arise from either the extracapsular or the intracapsular portion and radiate in spherical forms in all directions, as in Heliozoa. In Actipylea, myonemes are present in certain pseudopodia and produce circular groups of short, rod-like bodies clustered around each of the radial spines (Fig. 219, c). They connect the peripheral portion of the body with the pseudopodial covering of the spicule and possess a great contractile power, supposedly with hydrostatic function (p. 62).
skeletal structure of Radiolaria varies considerably from simcomplex and has a taxonomic value. The chemical nature of the skeleton is used in distinguishing the major subdivisions of the order. In the Actipylea it seems to be made up of strontium sulphate, while in the three other groups, Peripylea, Monopylea, and Tripylea, it consists fundamentally of siliceous substances. The skeleton of the Actipylea is sharply marked from others in form and structure. The majority of this group possess 20 rods radiating from center. The rod-shaped skeletons emerge from the body in most cases along five circles, which are comparable to the equatorial, two tropical and two circumpolar circles of the globe, which arrangement

The

ple to

is

known as Mutter's law, since J. Miiller first noticed it in 1858. The life-cyle of the Radiolaria is very incompletely known (Fig.
budding has been seen in some and Tripylea. Multiple division is also known Thalassophysidae in which it is the sole known means of

218). Binary or multiple fission or

Peripylea, Actipylea,
to occur in

518

PROTOZOOLOGY

line

The central capsule becomes very irregular in its outand the nucleus breaks up into numerous chromatin globules. Finally the capsule and the intracapsular cytoplasm become transreproduction.

Fig. 218. Diagram illustrating the probable life-cycle of Actipylea (Kiihn). a, mature individual; b, c, binary fission; d, e, multiplication by budding; f, mature individual similar to a; g, formation of swarmers; h-j,

supposed, but not observed, union of two swarmers producing a zygote;

k,
1,

young

individuals.

formed into numerous small bodies, each containing several nuclei. Further changes are unknown. Swarmer-formation is known in some forms. In Thalassicolla, the central capsule becomes separated from the remaining part of the body and the nuclei divide into a number of small nuclei, around each of which condenses a small ovoidal mass
of cytoplasm.

They soon develop

flagellum. In the

meantime the
its

capsule descends to a depth of several hundred meters, where

RADIOLARIA
wall bursts

519

and the flagellates are liberated (g). Both isoswarmers and anisoswarmers occur. The former often contain a crystal and a few fat globules. Of the latter, the macroswarmers possess a nucleus and refringent spherules in the cytoplasm. Some forms possess 2 flagella, one of which is coiled around the groove of the body, which makes them resemble certain dinoflagellates. Further development is unknown; it is supposed that the anisoswarmers are sexual and isoswarmers asexual generations. Nuclear relationship (Hertwig,
1930).

Enormous numbers
of the genera.

of species of Radiolaria are

known.

An

out-

line of the classification is

given below, together with a few examples,

Skeleton composed of strontium sulphate Suborder 1 Actipylea Skeleton composed of other substances Central capsule uniformly perforated, skeleton either tangential to the capsule or radiating without reaching the intracapsular region. Suborder 2 Peripylea (p. 520) Central capsule not uniformly perforated Capsule monaxonic, bears at one pole a perforated plate forming the base of an inward-directed cone Suborder 3 Monopylea (p. 522) Capsule with 3 openings: 1 astro pyle and 2 parapyles Suborder 4 Tripylea (p. 523)

Suborder

Actipylea Hertwig

Radial spines, 10-200, not arranged according to Midler's law. Spines radiate from a common center, ancestral forms (Haeckel).

Family

Actineliidae

Genus Actinelius
10-16 spines irregularly set

(Fig. 219, a)

Family 2 Acanthociasmidae
(Fig. 219, b)

Genus Acanthociasma
Without tangential skeletons Spines more or less uniform

Radial spines, few, arranged according to Midler's law

in size

Spicules circular in cross-section

Family 3 Acanthometridae
(Fig. 219, c)

Genus Acanthometron
Spicules cruciform in cross-section

Family 4 Acanthoniidae

Genus Acanthoma
2 opposite spines

(Fig. 219, d)

much

larger

Family 5 Amphilonchidae

520

PROTOZOOLOGY

"SPIT
Pfflg
Fig. 219. a, Actinelms primordialis, X25 (Haeckel); b, Acanthociasma planum, X65 (Mielck); c, Acanthometron elasticum (Hertwig); d, Aconthonia tetracopa, X40 (Schewiakoff ) e, Amphilonche hydrometrica, X130
;

(Haeckel);

f,

Hexaconus

serratus,

X100

(Haeckel).
(Fig. 219, e)

Genus Amphilonche
With tangential skeletons
20 radial spines of equal with one pore
size, shell

composed of small plates, each Family 6 Sphaerocapsidae

Genus Sphaerocapsa
2 or 6 larger spines 2 enormously large conical sheathed spines

Family

7 Diploconidae

Genus Diploconus
6 large spines

Family 8 Hexalaspidae
(Fig. 219, f)

Genus Hexaconus

Suborder 2 Peripylea Hertwig

Solitary, skeleton wanting or simple spicules; mostly spherical

Nucleus spherical with smooth membrane Vacuoles intracapsular

Family

Physematiidae

Genus Lampoxanthium
Vacuoles extracapsular

(Fig. 220, a)

Family 2 Thalassicollidae

Genus

Thalassicolla (Fig. 220, b)

Nuclear membrane not smoothly contoured Nuclear wall branching out into pouches, structure similar to the Family 3 Thalassophysidae last ......
,

RADIOLARIA

521

Fig. 220 a,

Lampoxanthium pandora, X20 (Haeckel);

nucleata,

b,

Thalassicolla

X15 (Huth).

Genus Thalassophysa
Nuclear wall crenate Huge double spicule

Family 4 Thalassothamnidae

Genus Thalassothamnus

latticed skeleton, with branching

and thorny spines Family 5 Orosphaeridae

Genus Orosphaera
Solitary, skeleton complex, often concentric

Central capsule and skeleton spherical

Family 6 Sphaeroidae

Genus Hexacontium

(Fig. 221, a)

Central capsule and skeleton elliptical or cylindrical

Family 7 Prunoidae
c

iri*

#^

c, e,

Fig. 221. a, Hexacontium aster acanthion, X130; b, Pipetta tuba, X100; Staurocyclia phacostaurus, X130; d, Cenolarus primordialis, X100;

SphaerQZoum ovodimare, X30 (Haeckel).

522

PROTOZOOLOGY
Genus Pipetta
(Fig. 221, b)

Central capsule and skeleton discoidal or lenticular

Family 8 Discoidae

Genus Staurocyclia
Similar to the above, but flattened

(Fig. 221, c)

Family
(Fig. 221, d)

9 Larcoidae

Genus Cenolarus

Colonial, individuals with anastomosing extracapsular cytoplasm, embedded in a jelly mass Without latticed skeleton, but with siliceous spicules arranged tangentially to central capsule Family 10 Sphaerozoidae

Genus Sphaerozoum

(Fig. 221, e)

Central capsule of each individual enclosed in a latticed skeleton Family 11 Collosphaeridae

Genus Collosphaera
Suborder 3 Monopylea Hertwig
Without any skeleton
Family
(Fig. 222, a)
1

Nassoidae

Genus Cystidium
With skeleton Without a complete

latticed skeleton

Skeleton a basal tripod

Family 2 Plectoidae

c,

Fig. 222. a, Cystidium princeps, X120; b, Triplagia primordialis, X25; Lithocircus magnificus, X100; d, Dictyophimus hertwigi, X80 (Haeckel).

Genus Triplagia

(Fig. 222, b)
.
.

Skeleton a simple or multiple sagittal ring.

Family 3 Stephoidae

Genus Lithocircus
With a complete
latticed skeleton

(Fig. 222, c)

Lattice skeleton single, without constriction.

Family 4 Cyrtoidae

Genus Dictyophimus
Lattice skeleton multiple

(Fig. 222, d)

Family 5 Botryoidae

RADIOLARIA
Genus Phormobothrys
Suborder 4 Triplylea Hertwig
Without skeleton; with isolated spicules

523

Skeleton consists of radial hollow rods and fine tangential needles Family 1 Aulacanthidae

Genus Aulacantha
With
foreign skeletons covering

(Fig. 223, a)

body surface Family

2 Caementellidae

Fig.

223.

a,

stapedia,

X65

(Haeckel);

Aulacantha scolymantha, X30 (Kuhn); b, Caementella c, Aulosphaera labradoriensis, XlO (Haecker).

Genus Caementella
With skeleton

(Fig. 223, b)

1-2 (concentric) usually spherical skeletons Outer lattice skeleton with triangular or areolar meshes Family 3 Sagosphaeridae

Genus Sagenoscene
One
lattice skeleton

with hollow radial bars

Family 4 Aulosphaeridae

Genus Aulosphaera

(Fig. 223, c)

2 concentric lattice skeletons connected by radial bars Family 5 Cannosphaeridae

Genus Cannosphaera
One
skeleton, simple, but variable in shape; bilaterally symmetrical Family 6 Challengeridae Skeleton with fine diatomaceous graining
.

Genus Challengeron

(Fig. 224, a)

Skeleton smooth or with small spines

Family

Medusettidae

524

PROTOZOOLOGY
Genus Medusetta
(Fig. 224, b)

One

skeleton; spherical or polyhedral, with an opening and with radiating spines Skeleton spherical or polyhedral, with uniformly large round pores Family 8 Castanellidae

Fig. 224. a, Challengeron wyvillei, X 105 (Haeckel) b, Medusetta ansata, (Borgert); c, Castanidium murraiji, X25 (Haecker); d, Circoporus octahedrus, X65 (Haeckel); e, Tuscarora murrayi, X7 (Haeckel); f, Coelo;

X230

aendrum ramosissimum, XlO (Haecker).

Genus Castanidium
Skeleton similar to the rounded by pores
last,

(Fig. 224, c)

but the base of each radial spine surFamily 9 Circoporidae

(Fig. 224, d)

Genus Circoporus

Skeleton flask-shaped with 1-2 groups of spines

Family 10 Tuscaroridae

Genus Tuscarora

(Fig. 224, e)

Central portion of skeleton consists of 2 valves Valves thin, each with a conical process which divides into branched Family 11 Coelodendridae tubes

Genus Coelodendrum

(Fig. 224,

f)

References

Brandt, K.: (1905) Zur Systematik der koloniebildenden Radiolarien. Zool.

Jahrb. Suppl., 8:311.

RADIOLAMA
Borgert, A.: (1902) Mitteilungen ueber

525

die Tripyleen-Ausbeute der Plankton-Expedition. I. Zool. Jahrb. Syst., 15:563. (1904) II. Ibid., 19:733. (1905) Die Tripyleen Radiolarien der Plankton-Expedition. Ergebn. Plankton-Exp. Humboldt-Stiftung, 3:95. (1913) II. Ibid., 3:539. Haeckel, E.: (1862) Die Radiolarien. Eine Monographic I.

(1887) II. (1887a) Report on the Radiolaria collected by H.M.S. Challenger. Chall. Rep. Zool., 18. Haecker, V.: (1908) Tiefseeradiolarien. Wiss. Ergebn. deutsch. Tiefsee-Exp., 14:337. Hertwig, R. (1879) Der Organismus der Radiolarien. Jena. (1930) Ueber die Kern verhaltnisse der Acanthometren. Arch. Protist., 71:33.
:

Chapter 24
Class 3 Sporozoa Leuckart
Sporozoa THE Their hosts
are without exception parasitic

and bear

spores.

are widely distributed in the animal kingdom, from

Protozoa to Chordata. As a rule, they are incapable of locomotion, but some when immature may move about by pseudopodia or myonemes. They possess neither cilia nor flagella, except in the gamete stage. In the forms that are confined to one host, the spore is usually enveloped by a resistant membrane which would enable it to
withstand unfavorable conditions while outside the host body, but
in those
is

naked. The method of nutrition

having two host animals, as in Plasmodium, the sporozoite is saprozoic or parasitic, the food
fluid,

being dissolved cytoplasm, tissue

material of the host.
species.

body

fluid, or

dissolved food

Both asexual and sexual reproductions are well known in many Asexual reproduction is by repeated binary or multiple fission or budding of intracellular trophozoites. The multiple division
in a host cell

produces far greater number

of protozoans belonging to other classes

schizogony.
fusion or

The sexual reproduction is autogamy and marks in many

of individuals than that and often is referred to as by isogamous or anisogamous

cases the beginning of

sporogony or spore-formation. Schaudinn (1900) divided the Sporozoa into two groups, Telosporidia and Neosporidia, and this scheme has been followed by several authors. Some recent writers consider these two groups as separate classes. This, however, seems to be improper, as the basis of distinction between them is entirely different from that which is used for distinguishing the other four classes: Sarcodina, Mastigophora, Ciliata, and Suctoria. For this reason, the Sporozoa are placed in a
single class

and divided into three subclasses

as follows:

Spore simple; without polar filament Spore with or without membrane; with 1-many sporozoites
Subclass
1

Telosporidia
(p. (p.

Spore with membrane; with one sporozoite Spore with polar filament
Subclass 2 Acnidosporidia Subclass 3 Cnidosporidia
1

635) 643)

Subclass

Telosporidia Schaudinn

The spore which ment possesses one

the trophic
life

contains neither a polar capsule nor a polar filato several sporozoites and is formed at the end of

of the individual. In the forms

which invade two host

526

SPOROZOA, GREGARINIDA

527

animals to complete their development, there occur naked sporozoites instead of spores.

The

infection of a

new host begins with the entrance

of

mature

spores through mouth, or with the introduction of the sporozoites

by blood-sucking invertebrates directly into the blood stream. The grow at the expense of the latter. In the Coccidia and the Haemosporidia, the trophozoite continues its intracellular existence, but in the Gregarinida it leaves the host cell and grows in an organ cavity. Except Eugregarinina, the vegetative form undergoes schizogony and produces a large number of daughter individuals which invade new host cells, thus
sporozoites enter specific host cells and there

spreading the infection within the host body.

nally develop into gametocytes. In the Coccidia

The

trophozoites

fi-

and the Haemosporidia, anisogametes are, as a rule, produced. Each macrogametocyte develops into a single macrogamete and each microgametocyte, into several microgametes. Fusion of the gametes in pairs results in formation of a large number of zygotes, each of which develops either into one to many spores or into a number of naked sporozoites. In the Gregarinida, two fully mature trophozoites (or gametocytes) encyst together and the nucleus in each multiplies repeatedly to form numerous gametes, which fuse in pairs with those produced in
the other individual within the

common

envelope.

velop into spores, each containing variable

The zygotes denumber of sporozoites.

above are

When

these spores enter a

new

host, the changes outlined

repeated.

The

Telosporidia are parasitic in vertebrates and higher

in this subclass:

invertebrates.

Three orders are distinguished

Mature trophozoite
enveloped

extracellular, large; zygote not motile; sporozoites

Order
intracellular, small
.

Gregarinida

Mature trophozoite

Zygote not motile; sporozoites enveloped. .Order 2 Coccidia (p. 570) .Order 3 Haemosphoridia (p. 599) Zygote motile; sporozoites naked.
.

Order

Gregarinida Lankester

The

gregarines are chiefly coelozoic parasites in invertebrates,

and annelids. They obtain their nourishment from the host organ-cavity through osmosis. The vast majority of gregarines do not undergo schizogony and an increase in number is carried on solely by sporogony. In a small group, however, schizogony takes place and this is used as the basis for grouping these protozoans into two suborders as follows:
especially arthropods

No schizogony Schizogony occurs

Suborder 1 Eugregarinina Suborder 2 Schizogregarinina

(p. (p.

528) 560)

528

PROTOZOOLOGY
Suborder
1

Eugregarinina Dofiein

This suborder includes the majority of the so-called gregarines which are common parasites of arthropods. When the spore gains entrance into a suitable host, it germinates and the sporozoites emerge and enter the epithelial cells of the digestive tract. There they grow at the expense of the host cells which they leave soon and to which they become attached by various organellae of attachment (Fig. 235). These trophozoites become detached later from the host cells and move about in the lumen of the gut. This stage, sporadin, is ordinarily most frequently recognized. It is usually large and vermiform. The body is covered by a definite pellicle and its cytoplasm is clearly differentiated into the ectoplasm and endoplasm. The former contains myonemes (p. 62) which enable the organisms to undergo gliding movements (Watson, 1916). In one group, Acephalina, the body is of a single compartment, but in the other group, Cephalina, the body is divided into two compartments by an ectoplasmic septum. The smaller anterior part is the protomerite and the larger posterior part, the deutomerite,
contains a single nucleus. In Pileocephalus (Fig. 236,
said to be located in the protomerite
s)

the nucleus

is

and according to Goodrich

(1938) both the protomerite and deutomerite of

Nina gracilis contain

a nucleus.

The endoplasm

contains numerous spherical or ovoidal

bodies which are called zooamylon or paraglycogen grains and

which are apparently reserve food material (p. 112). The protomerite may possess an attaching process with hooks or other
structures at
its

anterior border; this

is

called the epimerite.

The

epi-

merite

is

usually not found on detached sporadins. Goodrich obis

served recently that in Nina the protomerite the gregarine

a knob-like part of

when

contracted, but expands freely and used as a

mobile sucker for attachment to the gut epithelium of the host Scolopendra. Presently multiple filiform epimerite grows at the free edge of the sucker and penetrates between the host cells. Epimerite bearing trophozoites are called cephalins. Cytology (Gohre, 1943). Many gregarines are solitary, others are often found in an endwise

two or more sporadins. This association is called is known as the primite and the posterior, the satellite. What differences exist between the two individuals that become associated is not well known. But Muhl (1921) reported in Gregarina cuneata, the granules in the primite and the
association of

syzygy.

The

anterior individual

satellite stained differently

with neutral red. Sporadins usually en-

and become gametocytes. This process following biassociation was observed in a number of species; for example, in
cyst in pairs

SPOROZOA, GREGARINIDA

529

Leidyana erratica (Watson, 1916), Gregarina blaitarum (Sprague, 1941) (Fig-. 226), etc. Within the cyst-membrane, the nucleus in each individual undergoes repeated division, forming a large number of small nuclei which by a process of budding transform themselves into numerous gametes. The gametes may be isogamous or anisogamous. Each of the gametes in one gametocyte appears to unite with one formed in the other, so that a large number of zygotes are produced. In some species such as Nina gracilis the microgametes enter the individual in which macrogametes develop, and the development of zygotes takes place, thus producing the so-called pseudocyst. The zygote becomes surrounded by a resistant membrane and its content

culicis

Diagram illustrating the developmental cycle of Lankesteria (Wenyon). a, entrance of sporozoite into the mid-gut epithelium and growth of trophozoites; b, mature trophozoite found in the lumen of gut; c, association of two gametocytes prior to encystment; d-f, gamete formation; g, zygote formation; h, development of spores from zygotes; i, a spore; j, emergence of eight sporozoites from a spore in a new host
Fig. 225.
gut.

530

PROTOZOOLOGY

develops into the sporozoites, thus developing into a spore. The spores germinate when taken into the alimentary canal of a host

animal and the life-cycle is repeated. According to Wenyon, in a typical Eugregarinina, Lankesteria culicis (Fig. 225) of Aedes aegypti, the development in a new host begins when a larva of the latter ingests the spores which had been set free by infected adult mosquitoes in the water. From each spore
(j), which enter the epithelial cells of the stomach and grow (a). These vegetative forms leave the host cells later and become mingled with the food material present in the stomach lumen of the host (6). When the larva pupates, the sporadins enter the Malpighian tubules, where they encyst (c). The repeated nuclear division is followed by formation of large numbers of gametes (d-f) which unite in pairs (g). The zygotes thus formed develop into spores, each possessing 8 sporozoites (h). Meanwhile the host pupa emerges as an adult mosquito, and the spores which become set free in the lumen of the tubules pass into the intestine, from which they are discharged into water. Larvae swallow the spores and acquire infection.

are liberated 8 sporozoites

Eugregarinina are divided into 2 tribes

Trophozoite not septate Trophozoite septate

Tribe 1 Acephalina Tribe 2 Cephalina

(p. (p.

531) 541)

Fig. 226. Encystment in Gregarina blattarum, X60 (Sprague). a, a trophozoite with epimerite and 3 pairs of syzygy; b, association of three individuals; c-h, encystment as seen in a single pair in about one hour.

SPOROZOA, GREGARINIDA
Tribe
1

531

Acephalina Kolliker

The
spores

acephalines are mainly found in the body cavity and organs

it. The infection begins by the ingestion of mature by a host, in the digestive tract of which the sporozoites are set free and undergo development or make their way through the gut wall and reach the coelom or various organs such as seminal vesicles. Young trophozoites are intracellular, while more mature

associated with

forms are either intracellular or extracellular. Acephaline gregarines (Berlin, 1924; Bhatia and Chatterjee, 1925; Bhatia and Setna, 1926;
Bhatia, 1929; Troisi, 1933).
Spores with similar ends Spores biconical Sporadins solitary Anterior end not differentiated Anterior end conical or cylindro-conical

Family

Monocystidae
(p.

Family 2 Rhynchocystidae
.

534)

Sporadins in syzygy Spores with thickenings at ends Family 3 Zygocystidae (p. 534) Spores without thickenings. .Family 4 Aikinetocystidae (p. 535) Spores not biconical Family 5 Stomatophoridae (p. 536) Spores navicular Spores round or oval Family 6 Schaudinnellidae (p. 537) No encystment Family 7 Diplocystidae (p. 538) 2 sporadins encyst together Spores with dissimilar ends Family 8 Urosporidae (p. 538) Spores with epispore Family 9 Allantocystidae (p. 540) Spores without epispore SDores unobserved; grown trophozoites with cup-like depression at
.

posterior end for syzygy

Family 10 Ganymedidae
Biitschli

(p.

541)

Family

Monocystidae

Trophozoites spheroidal to cylindrical; anterior

entiated; solitary; spores biconical, without
rozoites.

end not

differ-

any

spines, with 8 spo-

Genus Monocystis Stein. Trophozoites variable in form; motile; incomplete sporulation in cyst; spore biconical, symmetrical; in coelom or seminal vesicles of oligochaetes. Numerous species (Berlin,
1924).

M.

ventrosa Berlin (Fig. 227, a-c). Sporadins 109-1 83m

;

by 72-

135m; nucleus up to 43m by 20m cysts 185-223m by 154-182u; spores 17-25m by 8-19m; in Lumbricus rubellus, L. castaneus and Helodrilus foetidus.

M. lumbrici Henle (Fig. 227, d, e). Sporadins about 200m by 60-70m; cysts about 162m in diameter; in Lumbricus terrestris, L.
rubellus,

and L. castaneus

(Berlin, 1924).

532

PROTOZOOLOGY
.

Elongate oval; average dimenend often drawn out into a process; pellicle thick, longitudinally striated; cysts about 750 /x in diameter; spores 23/x by 9ju," in the seminal vesicles of Lumbricus terrestris. Mulsow (1911) found vegetative stages in autumn and winter and sporogony in spring. Meiosis in the last pre-gametic division (p. 207).
rostrata
(Figs. 92, 228).

Mulsow

sions 450/z

by

220/x; anterior

Fig. 227. a-c,

(Berlin);
d,
e,

Monocyslis ventrosa
lumbrici,

(a,

X260;
f.

b,

X150;

c,

X830)

M.

X280

(Berlin);

Apolocystis gigantea,

X90
h,
(i,

(Troisi); g, A. minuta, with attached phagocytes, X770 (Troisi); Nematocystis vermicularis, X80 (Hesse); i, j, Rhabdocystis claviformis

X220;

j,

X270) (Boldt);

k,

1,

Enterocystis ensis (k,

X140) (Zwetkow).

principal axis

Genus Apolocystis Martiis. Trophozoites spherical; without marked by presence of any special peripheral organ;
coelom of various

solitary; spore biconical; in seminal vesicles or

oligochaetes.

Many species.
/).

A. gigantea Troisi (Fig. 227,

foetidus

In seminal vesicles of Helodrilus

and Lumbricus

rubellus; late

October to March only; fully

SPOROZOA, GREGARINIDA

533

grown trophozoites 250-800^ in diameter; whitish to naked eyes; pellicle thickly covered by 10-15/x long 'hairs'; endoplasm packed
with spherical paraglycogen grains (3m in diameter), nucleus 3543m in diameter; cysts 400-800m in diameter; spores 19m by 8.6m
(Troisi, 1933).

A. minuta Troisi (Fig. 227,

terrestris,

g).

L. castaneus and L. rubellus;

In seminal vesicles of Lumbricus mature trophozoites 40-

46m in diameter; endoplasm yellowish brown, packed with spherical paraglycogen grains (5.3-7m in diameter); nucleus 10m in diameter;
cysts 68-74m by 55-65m; spores of 3 sizes, 11m by 5.5m, 18.8m by 7m and 21.6m by 9.8m. Genus Nematocystis Hesse. Trophozoites elongate, cylindrical and shaped like a nematode; solitary. Many species^/ Bhatia*and

Chatterjee, 1925).

Fig. 228. Monocystis rostrata (Mulsow). a-c, trophozoites, X90; d, spore, X850.

N. vermicularis H.
terrestris,

(Fig. 227, h). In seminal vesicles of

Lumbricus

Pheretima barbadensis; trophozoites 1 mm. by 100m; cylindrical, both ends with projections; nucleus oval; endoplasm alveolated, with paraglycogen grains; sporadins become paired lengthwise; cysts and spores unknown. Genus Rhabdocystis Boldt. Trophozoites elongate, gently curved;
L.
rubellus,

Helodrilus longus,

anterior end swollen, club-shaped; posterior end attenuated; spores

with sharply pointed ends. One species. R. claviformis B. (Fig. 227, i, j). In seminal vesicles of Octolasium

complanatum; sporadins extended, up to 300m by 30m; pellicle distinctly longitudinally striated; zooamylon bodies 2-4m in diameter;
cysts biscuit-form, 110m

by 70m; spores 16m by 8mGenus Enterocystis Zwetkow. Early stages of trophozoites

in

syzygy; sporadins in association ensiform; cysts spherical without

ducts; spores elongate ovoid, with 8 sporozoites; in gut of ephemerid
larvae. Species (Noble, 1938a).

534

PROTOZOOLOGY
k, I).

E. ensis Z. (Fig. 227,

of Caenis sp.

Sporadins in syzygy 200-510/x long;

cysts 200-350yu in diameter; spores elongate ovoid; in gut of larvae

Genus Echinocystis Bhatia and Chatterjee. Body nearly spherical with two spine-like structures extending out from the body surface; solitary; spores biconical with equally truncated ends; in the seminal
earthworms (Bhatia and Chatterjee, 1925). Body 740 m by 65m; spines sometimes unequally long; observations on spores incomplete; in the sperm sacs of
vesicles of

E. globosa B. and C.

Pheretima heterochaeta.

Family 2 Rhynchocystidae Bhatia

Trophozoites ovoid, spherical or elongate, with a conical or cylindro-conical trunk at anterior end; solitary; spore biconical, with

8 sporozoites.

Genus Rhynchocystis Hesse. Trophozoites ovoid or

cles of oligochaetes.

cylindrical;

plastic epimerite, conical or cylindro-conical trunk; in seminal vesi-

Many

species (Bhatia

and Chatterjee, 1925;

Troisi, 1933).
a). In seminal vesicles of Lumbricus and Helodrilus foetidus; 217m by 25.5/*; pellicle with close, longitudinal ridges from which arise 'hairs' up to 40/i in length; endopLasm viscous, packed with oval (3m by 2m) paraglycogen bodies; cysts ovoid, 95m by 84/x; spores 13.3m by 5m

R. pilosa Cuenot (Fig. 229,

L. castaneus

terrestris,

(Troisi, 1933).

R. porrecta Schmidt (Fig. 229,

bricus rubellus

b, c).

In seminal vesicles of

Lum-

and Helodrilus foetidus; extremely long with an enlarged head; up to 2.5 mm. by 32-36m; sluggish; endoplasm granulated, filled with oval (4m by 2-3m) paraglycogen grains; nucleus 1725m in diameter; spores 27.7-28m by 12m; sporozoites 13-18m by 3-5m
(Troisi, 1933).

Family 3 Zygocystidae Bhatia

Trophozoites in association; spores biconical, with peculiar thickenings at extremities; with 8 sporozoites; in seminal vesicles or coe-

lom of oligochaetes. Genus Zygocystis

Stein.

Sporadins pyriform, 2-3 in syzygy; in

seminal vesicles or coelom of oligochaetes. Several species. Z. wenrichi Troisi (Fig. 229, d, e). In seminal vesicles of Lumbricus

and Helodrilus foetidus; sporadins up to 1.5 mm. by 250m in diameter; pellicle with longitudinal ridges which become free and form a 'tuft of hairs' at the posterior end; cysts 500-800m by 300500m; spores 28m by 13m.
rubellus

SPOROZOA, GREGARIXIDA

535

Genus Pleurocystis Hesse. Trophozoites in longitudinal or lateral association; spores biconical. One species. P. cuenoti H. (Fig. 229, /). In the ciliated seminal horn of Helodrilus longus and H. caliginosus; 2 mm. by 300//; pellicle striated
longitudinally, obliquely near the posterior end; cysts 1.5-2

mm.

in

diameter; spores 28. m by

12/x

(Hesse, 1909).

Family 4 Aikinetocystidae Bhatia

Trophozoites solitary or in syzygy; branching dichotomously, branches with sucker-like organellae of attachment; spores biconical.

Fig. 229 a, Rhynchocystis pilosa, X200 (Hesse); b, c, R. porrecta: X170 (Hesse); c, spore, X1330 (Troisi); d, e, Zygocystis wenrichi (d, X45; e, X450) (Troisi); f, Pleurocystis cuenoti, X190 (Hesse); g, h, Aikinetocystis singularis (h, X320) (Gates); i-k, Stomatophora coronata (i, j, X430; k, X870) (Hesse); 1, Astrocystella lobosa, X120; m, Craterocystis papua, X65; n, Choanocystella tentaculata, X570; o, Choanocystoides costaricensis, X470 (Martiis).
b,

536

PROTOZOOLOGY

Genus Aikinetocystis Gates. Trophozoites cylindrical or columnar, with a characteristic, regular dichotomous branching at attached end, with sucker-like bodies borne on ultimate branches; solitary or
2 (3-8) individuals in association; spores biconical.

A. singularis G. (Fig. 229, g, h). In coelom of Eutyphoeus foveatus. E. rarus, E. peguanus and E. spinulosus (of Burma) trophozoites up
;

to 4

mm.

long;

number

of branches 8 or 16, each with

an irregular

sucker; ovoid nucleus near rounded end; spores of two sizes, 20-23m long and 7-8m long; a few cysts found, ovoid and about 600m long.

Family 5 Stomatophoridae Bhatia

Trophozoites spherical to cylindrical or cup-shaped with a suckerends truncate; 8 sporozoites; in seminal vesicles of Pheretima (Oligochaeta)
;

like epimerite; solitary; spores navicular,

Genus Stomatophora Drzewecki. Trophozoites

spine; spores navicular. Several species.

spherical or ovoid:

anterior end with a sucker-like epimeritic organella with a central

S. coronata (Hesse) (Fig. 229, i-k). In seminal vesicles of Pheretima rodericensis, P. hawayana and P. barbadensis; trophozoites spherical, ovoid or elliptical, about 180m by 130m; endoplasm with

ovoid paraglycogen grains; cysts ellipsoid or fusiform, 70-80 m by

in 2 sizes, 11m by 6m and 7m by 3m and in chain. Genus Astrocystella Martiis. Trophozoites solitary; stellate with 5-9 lobes radiating from central part containing nucleus; anterior surface with a depression. One species.

50-60m; spores

fortii

A. lobosa M. (Fig. 229, I). In seminal vesicles of Pheretima beau(New Guinea) diameter about 200m; spores fusiform. Genus Craterocystis M. Trophozoites solitary; rounded; a suckerlike depression on anterior end; myonemes well developed, running
;

from concave to convex

C.

side.

One

species.

In prostate and lymphatic glands of Pheretima wendessiana (New Guinea); trophozoites about 360(Fig. 229, m).

papua M.

390m in diameter. Genus Choanocystella M. (Choanocystis M.). Trophozoites solitary; rounded or ovate; anterior end with a mobile sucker and a tentacle bearing cytoplasmic hairs; myonemes. One species. C. tentaculata M. (Fig. 229, n). In seminal vesicles of Pheretima beaufortii (New Guinea) trophozoites 50m by 36mGenus Choanocystoides M. Trophozoites solitary, rounded or cupshaped; anterior end with a mobile sucker, bordered by cytoplasmic
;

filaments.

One

species.

C. costaricensis

M.

(Fig. 229, o). In

seminal vesicles of Pheretima

SPOROZOA, GREGARINIDA

537

heterochaeta (Costa Rica); trophozoites 40-45/x in diameter; nucleus

ovoid, large, 12/x in diameter.

Genus Beccaricystis M. Mature trophozoites

one species.
B. loriai

elongate, cylindrical,
its

with a sucker-like depression at anterior end; nucleus at

bottom,
ser-

M.

(Fig. 230, a).

In seminal vesicles of Pheretima

mowaiana; trophozoites

cylindrical, with wart-like growths,

myo-

Fig. 230. a, Beccaricystis loriai, X570 (Cognetti); b, c, Schaudinnella henleae (b, X885; c, X1000) (Nusbaum); d, e, Diplocystis schneideri
(d, Xl4;e, spore, X2000) (Kunstler) f Urospora chiridotae, X200 (Pixell-Goodrich); g-i, Gonospora minchini (g, a young trophozoite in host egg; h, a mature trophozoite, X330; i, sporadins in association, X80) (Goodrich and Pixell-Goodrich).
; ,

nemes run lengthwise with

lOO/i long.

radially arranged transverse fibrils about

;

Genus

terior sucker

M. Mature trophozoites cup-shaped, with anwith a smooth wall; nucleus at its bottom. One species. A. crater C. In seminal vesicles of Pheretima sermowaiana.
Albertisella

Family 6 Schaudinnellidae Poche

Parasitic in the digestive system of oligochaetes; spores spherical;

trophozoites do not encyst; male trophozoites producing microgam-

538
etes

PROTOZOOLOGY
and female, macrogametes
;

zygotes or amphionts (spores)

rounded.

Genus Schaudinnella Nusbaum. Trophozoites elongate spindle, lumen or attached to gut wall; sporadins male or female; spherical macrogametes and fusiform microgametes zygotes or
free in
;

amphionts encapsulated, passed out of host or enter gut epithelium, dividing to produce many sporozoites (autoinfection). S. henleae N. (Fig. 230, b, c). In gut of Henlea leptodera; mature trophozoites about 70/x by 9/i; attached trophozoite with a clear wart-like epimerite; female and male sporadins; macrogametes,
5-7.5^
in

diameter; microgametes,

spindle-form,

1-1.25/*

long;

sporozoites rounded oval, 2.5-3/* in diameter.

Family 7 Diplocystidae Bhatia

Coelomic or gut parasites of insects; trophozoites solitary or associated early in pairs; spores round or oval, with 8 sporozoites. Genus Diplocystis Kunstler. Trophozoites spherical to oval; association of 2 individuals begin early in spherical form; spores round or oval, with 8 sporozoites; in the intestine and coelom of insects. D. schneideri K. (Fig. 230, d, e). In the body cavity of Periplaneta americana; young stages in gut epithelium; cysts up to 2 mm. in diameter; spores 7-8/* in diameter; sporozoites 8/i long. Meiosis (p.

208).

Genus Lankesteria Mingazzini. Trophozoites more or less spatulate; spherical cyst formed by 2 laterally associated sporadins in
rotation; spores oval, with flattened ends, with 8 sporozoites; in the

gut of tunicates, flatworms and insects. Several species. L. culicis (Ross) (Fig. 225). In gut and Malpighian tubules of Aedes aegypti and A. albopictus; mature trophozoites about 150200/z

by

3 1-4 1/t ; cysts spherical, in Malpighian tubules of host,

about

30/i in

diameter; spores

10/t

by

6/t.

Family 8 Urosporidae Woodcock

Coelomic parasites in various invertebrates; sporadins associative;
spores with unequal ends; with or without epispores of various forms,

with 8 sporozoites. Genus Urospora Schneider. Large; frequently in lengthwise association of 2 individuals of unequal sizes, spores oval, with a filamentous process at one end; in body cavity or blood vessel of Tubifex,

Nemertinea, Sipunculus, Synapta, and Chiridota. Several species. U. chiridotae (Dogiel) (Fig. 230, /). In blood vessel of Chiridota laevis (in Canada); paired trophozoites up to about 1 mm. long; with
stiff 'hairs'

(Goodrich, 1925).

SPOROZOA, GREGARINIDA

539

U. hardyi Goodrich. In the coelom of Sipunculus nudus; spores

about 16m long, process 4-6m long, with eight sporozoites; thinwalled cysts 0.5-2
cells of cysts

by

mm.

mm. in diameter; active phagocytosis by host and some trophozoites, producing brownish masses, or more in diameter, which are crowded together in the

posterior region of the host.

Genus Gonospora Schneider. Trophozoites polymorphic, oval, pyriform or vermiform; cysts spherical; spore with a funnel at one end, rounded at the other; in gut, coelom or ova of polychaetes.
G. minchini Goodrich and Pixell-Goodrich (Figs. 230, g-i; 231, g). In coelom of Arenicola ecaudata; young trophozoites live in host eggs which float in the coelomic fluid; fully grown trophozoites leave eggs in which they grow up to 200m long, and encyst together in pairs; spores without well-developed funnel, 8-10ju long (Goodrich and Goodrich, 1920).

Genus Lithocystis Giard. Trophozoites large, ovoid or cylindrical; attached for a long period to host tissue; pellicle with hairlike processes;

a long process at one end

dota laevis; fully
ter;

endoplasm with calcium oxalate cystals; spores ovoid, with in coelom of echinids.
;

L. brachycercus Goodrich (Fig. 231,

a, b).

In the coelom of Chiri-

grown spherical trophozoites up to 200m in diamespores with a short flattened tail; in Canada (Goodrlih, 1925).

L. lankesteri G. In the coelom of Sipunculus nudus; trophozoites covered with spinous structures; biassociative; spores 12-14/z by 6-8m; the long ribbon-like tail 50-60 m long.

or solitary; free end

Genus Pterospora Racovitza and Labbe. Sporadins associative drawn out into 4 bifurcated processes; cysts spherical or oval; spores with epispore drawn out into 3 lateral
processes; in coelom of polychaetes.

P. maldaneorum R. and L. (Fig. 231,

lus liopygue; trophozoites

epispore 24/x in

c, d). In coelom of Liocephaabout 140m long; cysts 288m, by 214m; diameter; endospore 10-14/* by 3-4/j.

Genus Ceratospora Leger. Sporadins elongate conical, head to head association; without encystment; spores oval with a small collar at one end and 2 divergent elongate filaments at other. One
species.

C. mirabilis L. (Fig. 231,

e,

/).

Sporadins 500-600m long; spore

by 8m, filaments 34m long; in general body cavity of Glycera sp. Genus Cystobia Mingazzini. Trophozoites, large, irregular; fully grown forms always with 2 nuclei, due to early union of 2 individuals; spores oval, membrane drawn out and truncate at one end; in blood vessels and coelom of Holothuria.
12m

540

PROTOZOOLOGY
d

Fig. 231. a, b, Lithocystis brachycercus, X1330 (Pixell-Goodrich); c, d, Pterospora maldaneorum (c, X40; d, X530) (Labbe); e, f, Ceratospora mirabilis (e, X45; f, X670) (Leger); g, Gonospora minchini, X2000 (Goodrich); h, i, Cystobia irregularis (h, X65; i, X770) (Minchin); j-m,
Allantocystis dasyhelei (j-1, anaspides, X570 (Huxley).

X500; m,

X560)

(Keilin);

n,

Ganymedes

C. irregularis (Minchin) (Fig. 231, h, ^.Trophozoites irregular in form; up to 500^ long; endoplasm opaque, granulated; cysts in connective tissue of vessels; spore ovoid, epispore bottle-like, 25/u long; in blood vessel of Holothuria nigra.

Family 9 Allantocystidae Bhatia

Trophozoites elongate cylindrical; cysts elongate, sausage-like;
spores fusiform, sides slightly dissimilar.

Genus

Allantocystis Keilin. Sporadins, head to head association;

cysts sausage-like; in dipterous insect.

One

species.

A. dasyhelei K. (Fig. 231, j-m). In gut of larval Dasyhelea obscura;

SPOROZOA, GREGARINIDA
full-grown sporadins 65-75/t

541

by

20-22/t; cysts 140-150/1

by

20/z;

spores 18m by 6.5/i (Keilin, 1920).

Family 10 Ganymedidae Huxley

Trophozoites only known; mature individuals biassociative; posterior end of primite with a cup-like depression to which the epimeritic organella of satellite

Genus Ganymedes Huxley. Characters

considers
it

as

unknown. Huxley an intermediate form between Acephalina and

fits;

cysts spherical; spores

of the family;

Cephalina.
G. anaspides

H.

(Fig. 2,31, n). In gut

and liver-tube

of the crus-

tacean, Anaspides tasmaniae (of Tasmania); trophozoites in association. 70-300/i

by

60-130/x; cysts 85-1 15/z in diameter.

Tribe 2 Cephalina Delage

is divided into the protomerite and deutomerite by an ectoplasmic septum; inhabitants of the ali-

The body

of a trophozoite

mentary canal of invertebrates, especially arthropods. Taxonomy and distribution (Watson, 1916; Pinto, 1919; Kamm, 1922, 1922a).
One host
species involved None-septate; epimerite a knob Septate

Family

Lecudinidae

(p.

542)

Development

intracellular

Sporadins associative Sporadins solitary

Family 2 Cephaloidophoridae Family 3 Stenophoridae

(p. (p.

543) 544)

Development

extracellular

Sporadins associative Satellite non-septate

Satellite septate

Family 4 Didymophyidae (p. 544) Family 5 Gregarinidae (p. 544)

Sporadins solitary Epimerite simple knob-like Cysts with several ducts Family 6 Leidyanidae Cysts without or with one duct

(p.

547)
548)

Family 7 Monoductidae

(p.

Two

Epimerite not simple knob-like Epimerite cup-shaped or digitate Epimerite cup-shaped. .Family 8 Menosporidae (p. Epimerite digitate. .Family 9 Dactylophoridae (p. Epimerite otherwise Spore hat-shaped Family 10 Stylocephalidae (p. Spore of other shapes Spore with spines. .Family 11 Acanthosporidae (p. Spore without spines Family 12 Actinocephalidae (p. host species involved Family 13 Porosporidae (p.
.
. .

549) 550) 552)

554)

554) 558)

542

PROTOZOOLOGY
Family
1

Lecudinidae

Kamm
spores
ovoidal,

Epimerite

simple,

symmetrical;

non-septate;

thickened at one pole; solitary; in gut of polychaetes and termites.

Undoubtedly intermediate forms between Acephalina and Cephalina.

Genus Lecudina Mingazzini. Epimerite

polychaetes. Species

simple,

knob-like; in

(Kamm,

1922).

Lecudina pellucida (Kolliker); b, Polyrhabdina spionis, c, Sycia inspinata (L6ger); d, e, Zygosoma globosum (d, X60; e, X1260) (Noble); f, Cephaloidophora olivia, X190 (Kamm); X50 (Leidy); h, S. robusta, X130 (Ellis); i, j, g, Stenophora larvata, Fonsecaia polymorpha (i, X220; j, X430) (Pinto); k, Gregarina blattarum, X55 (Kudo); 1, G. locustae, X65 (Leidy); m, G. oviceps, X30 (Crawley); n, Protomagalhaesia serpentula, X35 (Pinto); o, Gamocystis tenax (SchneiFig. 232.
a,

X800 (Reichenow);

der).

SPOROZOA, GREGARINIDA
L. pellucida (Kolliker) (Fig. 232, a). In Nereis cultrifera

543

and N.
1913).

beaucourdrayi ; trophozoites ellipsoid; spores

7/i

by

5/i (Ellis,

Genus Polyrhabdina Mingazzini. Trophozoites flattened, ovoidal; epimerite with a corona of processes with split ends, deeply stainable; in polychaetes (Spionidae).

P. spionis (Kolliker) (Fig. 232,

b).

In Scololepis fuligionosa;

100/*

by 35/t; epimerite with a corona of 8-10 processes; cysts unknown. Mackinnon and Ray (1931) report var. bifurcata, the epimerite of which is a "knob-shaped structure with a circlet of 14 to 16 minute teeth at its base, and at its crown, two much larger, diverging, clawlike processes."

intracellular; 2-14 sporadins in association; cysts

Genus Kofoidina Henry. Epimerite rudimentary; development and spores un1933).

known (Henry,
K.
ovata

H. In midgut of Zootermopsis angusticollis and Z. nevadensis; syzygy 153-672/* long; sporadins 41-105// long. Genus Sycia Lger. Epimerite knobbed, bordered by a thick ring;
protomerite subspherical
clusions; in

deutomerite conical, with navicular inmarine annelids (Leger, 1892). S. inspinata L. (Fig. 232, c). In Audouinia lamarcki. Genus Zygosoma Labbe. Trophozoites with wart-like projections; epimerite a simple knob; spores oval; in gut of marine annelids. Z. globosum Noble (Fig. 232, d, e). Trophozoites 250-500/t by 200-380/i epimerite a large globule; cysts 400/t by 360/i, without ducts; spores oval, with 4 sporozoites, 9/i by 7/i; reduction zygotic, 12 to 6 chromosomes; in gut of Urechis caupo in California. Genus Ulivina Mingazzini. Elongate ellipsoid; epimerite simple; spores unknown; in gut of polychaetes. U. rhynchoboli (Crawley). Sporadins up to 700 /i long; in the gut of Rhynchobolus americanus (Crawley, 1903).
; ;

Family 2 Cephaloidophoridae

Kamm
without spobiassociative,

Development

intracellular; early association; cysts

roducts; spores ovoidal, with equatorial line; in gut of Crustacea.

Genus Cephaloidophora Mawrodiadi. Sporadins

chain, ovoidal.

early; epimerite rudimentary; cysts without sporoducts; spores in

C. olivia (Watson) (Fig. 232/,). Biassociated sporadins

up

to 218/t

long; individuals
ter; spores (?)
;

diamegut of Libinia dubia; Long Island. C. nigrofusca (Watson). Sporadins, ovoid to rectangular, up to
to 118/i
36/t; cysts spheroidal, 60/t in

up

by

in

125/i

by

75/x;

cysts

and spores

(?); in

gut of Uca pugnax and U.

pugilator.

544

PROTOZOOLOGY
Family 3 Stenophoridae Leger and Duboscq

Development

intracellular;

sporadins solitary; with

a simple

epimerite or none; cysts open by rupture; spores ovoid, with or without equatorial line, not extruded in chain; in Diplopoda.

Genus Stenophora Labbe. With or without simple epimerite;

spores ovoid with equatorial
1916; Pinto, 1919).
S. larvata (Leidy) (Fig. 232, g). Sporadins up to 800m by 23m protomerite small; in gut of Spirobolus spinigerus. S. robusta Ellis (Fig. 232, h). Sporadins 140-180/x by 67m; cysts and spores both unobserved; in gut of Parajulus venustus, Orthomorpha
;

line,

not in chain. Species (Watson,

gracilis

and 0. sp.; Colorado. Genus Fonsecaia Pinto. Spores elongate ovoid; without equaF. polymorpha Pinto (Fig. 232,
i,

torial line.
j).

Sporadins 170m long; spores

18m

by

8m; in gut of Orthomorpha gracilis; Brazil.

Family 4 Didymophyidae Leger

Two

to three sporadins in association; satellite without septum.

cysts spherical,

Genus Didymophyes Stein. Epimerite a small pointed papilla; open by rupture; spores ellipsoidal. D. gigantea S. Sporadins slender, 1 cm. by 80- 100m; 2 deutomerites; cysts spherical, 600-700m in diameter; spores oval, 6.5m by
and Phyllognathus

6m; in gut of larvae of Oryctes nasicornis, O. sp.,

sp. (Leger, 1892).

Family 5 Gregarinidae Labbe'

Sporadins in association; epimerite simple, symmetrical; cysts
with or without ducts; spores symmetrical.

Genus Gregarina Dufour. Sporadins

biassociative;

epimerite

small, globular or cylindrical; spores dolioform to cylindrical; cysts

open by sporoducts; in the gut of arthropods. Numerous species (Watson, 1916). Morphology and physiology (Muhl, 1921). G. blattarum Siebold (Figs. 226; 232, k). Sporadins in syzygy, 5001100m; by 160-400m; cysts spherical or ovoidal; eight to 10 sporoducts; spores cylindrical to dolioform, truncate at ends, 8-8. 5m by 3.5-4m; in the midgut of cockroaches, especially Blatta orientalis. Reproduction (Schiffmann, 1919; Sprague, 1941).
G. locustae Lankester (Fig. 232,
Dissosteria Carolina.
G. oviceps Diesing (Fig. 232, m). Sporadins
I).

Sporadins 150-350m long: in

syzygy; spherical cysts 250m

in

up to 500m by 225m; in diameter; two to five sporoducts up

SPOROZOA, GREGARINIDA
to
1

545

mm.

long; spores dolioform, 4.5m

by 2.25m;

in Gryllus abbrevia-

te and

G. americanus (Leidy, 1853).

G. polymorpha (Hammerschmidt). Cylindrical sporadins up to 350m by 100m; in syzgyy; protomerite dome-shaped; deutomerite cylindrical, rounded posteriorly; a small nucleus with an endosome; in the intestine of larvae and adults of Tenebrio molitor ("meal worm"). G. rigida (Hall). Sporadins 28m by 20m up to 424m by 196m," syzygy; spherical cysts 212-505m in diameter; in the species of Melanoplus

(grasshoppers) (Kararo, 1920; Allegre, 1948).

Genus Protomagalhaesia

Pinto. Sporadins cylindrical; in syzygy,

protomerite of satellite draws in the posterior end of primite; cysts without ducts; spores dolioform, with spines at ends.
P. serpentula (Magalhaes) (Fig. 232, n). Sporadins up to 1.2

mm.

by 180m; in gut and coelom of Blatta orientalis. Genus Gamocystis Schneider. Septate only
ducts; spores cylindrical.

in trophozoites; spo-

radins non-septate; in syzygy; spore formation partial; with sporo-

A few species.
head to head; spherical cysts

G. tenax S. (Fig. 232, 6). Association

with 15 or more ducts; spore cylindrical, with rounded ends; in gut of Blattella lapponica (Schneider, 1875).

Genus Hyalospora Schneider. Sporadins

spores fusiform.
ter; spores 8.7m

in

syzygy; cytoplasm

yellowish orange; epimerite a simple knob; cysts open

by rupture;

Trophozoites 300m long; cysts, yellow, 60m in diameby 6m; in gut of Machilis cylindrica (Labbe, 1899). Genus Tettigonospora Smith. Similar to Hyalospora, but cytoplasm opaque white; spores spherical. One species (Smith, 1930). T. stenopelmati S. Sporadins 225-542m by 118-225m; spherical cysts 434-551 m in diameter, wall 17-66m thick; spores 4.8-5m in diaffinis S.

H.

ameter; in the midgut

of

Stenopelmatus fuscus and S. pictus ("Jerusa-

lem

crickets").

Genus Hirmocystis Labbe. Sporadins associative, 2-12 or more; with a small cylindrical papilla-like epimerite; cysts without ducts;
spores ovoidal.
to 1060m; sporadins

H. harpali Watson (Fig. 233, a). Total length of association up up to 560m by 80m; cysts unknown; in gut of Harpalus pennsylvanicus erythropus (Watson, 1916). H. termitis (Leidy) (Fig. 233, 6). Association 614-803m long;
epimerite simple sphere; cysts rare; spores (?); in Zootermopsis
angusiicollis, Z. ?ievadensis, etc.

(Henry, 1933).
in syzygy; deutomerite

Genus Uradiophora Mercier. Sporadins

546

PROTOZOOLOGY

X50 (Watson); b, H. termitis, X85 X270 (Vincent); d, e, Carcinoecetes hesperus (d, X200; e, X780) (Ball); f, Leydiana erratica, X170 (Watson); g-i, Lepismatophila thermobiae (g, h, X85; i, spores, X200) (Adams
Fig. 233.
a,

(Henry);

c,

Hirmocystis harpali, Anisolobus dacnecola,

and Travis); j-1, Colepismatophila watsonae (j, k, X85; 1, spores, X200) (Adams and Travis) m-o, Monoductus lunatus (m, cephalin, X240; n, C} st, X120; o, two views of spore, X2330) (Ray and Chakravatry).
;

with small process; epimerite an elongate papilla; cysts oval without

ducts; spores spherical, in chains (Mercier, 1911).

U. cuenoti

M.

(Fig. 234, a).

up
of

to 700/z long; cysts ovoid, 44 /i long; spores

2-4 sporadins in syzygy; individuals 4/x in diameter; in gut

biassociative; epimerite

Atyaephrya desmaresti.

Genus Pyxinioides Tregouboff. Sporadins

with 16 longitudinal furrows, small cone at end. P. balani (Kolliker). Primite up to 130^; satellite
of Balanus amphitrite

60ju long; in

gut

and B. eburneus.

ing; protomerite of primite

Genus Anisolobus Vincent. Sporadins in syzygy; epimerite lackexpanded to form sucker-like organella*

SPOROZOA, GREGARINIDA
cysts ellipsoid,

547

with thick envelope; with 6-8 sporoducts; spores

barrel-shaped.

One

species.

A. dacnccola V. (Fig. 233, c). In the midgut of the coleopteran Dacne rufifrons; 2 sporadins in syzygy 1 00-300 m by 20-50^; cysts without envelope, 130-150 n by 80-90/*; sporoducts 40-50/x long;
spores in chain, dolioform, 6> by 4^ (Vincent, 1924).

Genus Carcinoecetes
round to ovoidal, not
ins

Ball.

Sporadins in syzygy of 2 or more indigut of Crustacea (Ball, 1938). 2-6 sporadins in association; sporad-

viduals; epimerite rudimentary; cysts without sporoducts; spores

in chain; in
e).

C. hesperus B. (Fig. 233, d,

of hindgut; spores 8.6/i

in

320^ by 9m cysts about 140/i by 123^, attached to the wall by 7.7/z, with 8 radially arranged sporozoites; gut of the striped shore crab, Pachygrapsus crassipes; in California, C. bermudensis B. In the mid- and hind-gut of Pachygrapsus trans-

up

to

versus; in

Bermuda

(Ball, 1951).

Bermuda. Bermuda. Genus Heliospora Goodrich. Elongated, septate; spores more or

C. mithraxi B. In the gut of Mithr ax forceps; in
C. calappae B. In the gut of

Calappa flammca;

in

less spherical,

H. longissima (Siebold) form, up to 228m long; no

with equatorial ray-like processes (Goodrich, 1949). (Fig. 234, b-e). Trophozoites elongate filiintracellular stage; epimerite small,
roll

and

is

encystment; spherical cyst thinly walled and ruptures easily; microgametes flagellated; spores 7-8/x in diameter, with eight sporozoites and bear six long ray-like
retained until the sporadins
for

up

processes at the equator; in the gut of

Gammarus

pulex.

Genus Rotundula Goodrich. Rotund; button-like epimerite;

subspherical (Goodrich, 1949).
flagellate, 4/z in

pre-

cocious association; cyst without duct; spores, small, spherical or

R. gammari (Diesing) (Fig. 234,/). Cysts 40-50^; microgametes diameter; spores spherical, 5-6^ in diameter; in the

gut of

Gammarus

pulex.

Family 6 Leidyanidae
Similar to the last two families; but sporadins are solitary and

epimerite simple knob-like; cysts with several sporoducts.

Solitary; epimerite a simple globular knob; cysts with ducts; spores dolioform (Watson, 1915). L. erratica (Crawley) (Fig. 233,/). Sporadins up to 500^ by 160/x; cysts about 350^ in diameter; membrane about 30/x thick; 1-12 sporoducts; spores extruded in chains, 6/z by 3^; in gut of Gryllus

Genus Leidyana Watson.

sessile

abbreviatus

and G. pennsylvanicus.

548

PROTOZOOLOGY
Family 7 Monoductidae Ray and Chakravatry

As

in the last family solitary;

but cyst with a single sporoduct or

none; spore with 8 sporozoites. Genus Monoductus R. and C. Sporadins solitary; epimerite a small elevation with prongs attached to its base; anisogamy; cyst

with a single sporoduct; spores flattened fusiform, with dissimilar ends, each with 8 sporozoites. One species. M. lunatus R. and C. (Fig. 233, m-o). Cephalins 225-445/* by 33-4 7/x; epimerite with about 16 prongs; nucleus parachute-shaped, with

myonemes attached

at posterior margin; sporadins develop

posterior pseudopodial processes before association; cysts spherical,

225-230m in diameter, voided by host; development completed in 3-4 days outside the host body, with one duct; spores 10.25m by 4/x, truncate at one end, attenuated at other and discharged in a single chain; in gut of Diplopoda sp. Genus Sphaerocystis Leger. Sporadins solitary; without protomerrite; spherical.

S. simplex L. Sporadins 100-140/z in diameter; protomerite in

young trophozoites;

spherical cysts in which individuals are not

by 7.5m; in gut of Cyphon pallidulus. Genus Lepismatophila Adams and Travis. Epimerite a simple
associative, 100m in diameter; spores ovoid, 10.5m

knob; cysts without ducts; spores

species

ellipsoidal,

smooth, in chain. One

Sporadins 67-390^ by

(Adams and

Travis, 1935).

L. thermobiae A.

and T.

(Fig. 233, g-4).

30-174ju; cysts white to black, ellipsoidal to subspherical, 244-378/z

by

firebrat,

171-262ju; spores brown, 13.6m Thermobia domestica.

by

6.8m; in the ventriculus of the

to the last

Genus Colepismatophila Adams and Travis. Similar

genus; but larger; spores in
C. watsonae A.

wavy

chains, hat-shaped, with 2 curved

filamentous processes attached at opposite ends.

One

species.

Sporadins 92-562m by 55189m; cysts 226-464/i by 158-336m; spores 16.5m by 9.7m, processes 21m long; in ventriculus of Thermobia domestica (Adams and Travis, 1935). Genus Hyalosporina Chakravarty. Sporont solitary; epimerite

and T.

(Fig. 233, j-l).

small, tongue-like; anisogametes; cyst without ducts; spores oval,

with a hyaline membrane. One species (Chakravarty, 1935, 1936XH. cambolopsisae C. (Fig. 234, g-j). Trophozoites 247-1 11 1m by 37-1 11m; cysts oval, 292-390m by 263-375m; spores 8m; by 6m; in the
gut of the milliped, Cambolopsis
sp.

SPOROZOA, GREGARINIDA

549

Fig. 234. a, Uradiophora cuenoti in syzygy, X65 (Mercier); b-e, Heliospora longissima (Goodrich) (b, a pair in syzygy, X330; c, microgamete; d, zygote; e, a spore with 4 nuclei, X2665) f, Rotundula gammari in syzygy, X330 (Goodrich); g-j, Hyalosporina cambolopsisae (Chakravarty) (g, intracellular trophozoite, XI 110; h, a mature individual with fibrils tethering the nucleus, X120; i, anterior part of an attached organism, X2330; j, a spore, X1110); k, the digestive tube of Nepa cinerea with eight trophozoites attached to the stomach (opened) epithelium and three cysts of Coleorhynchus heros (Poisson).
;

Family 8 Menosporidae Leger

Sporadins solitary; epimerite a large cup, bordered with hooks, with a long neck; cysts without sporoducts; spores crescentic, smooth.

Genus Menospora Leger. With the characters

M.

polyacantha L. (Fig. 235,

a,

6).

of the family. Sporadins 600-700/* long;

in

cysts 200/x in diameter; spores 15^

by

4/z;

gut of Agrion puella.

550

PROTOZOOLOGY
Family 9 Dactylophoridae Leger

Sporadins solitary; epimerite complex, digitate; cysts dehiscence by pseudocyst; spores cylindrical; in gut of chilopods. Genus Dactylophorus Balbiani. Protomerite wide, bordered by
digitiform processes; spores cylindrical.

D. robustus Leger (Fig. 235,

hortensis.

c,

d).

spherical, 200/x in diameter; spores 11m

Sporadins 700-800/x long; cysts by 4.3/*; in gut of Cryptops

Genus Echinomera Labbe. Epimerite an eccentric cone with 8 or more digitiform processes; cysts without sporoducts; spores cylindrical.

E. magalhaesi (Pinto) (Fig. 235,

in gut of Scolopendra sp.

e).

Sporadins up to 300m by 70m;

spherical, with 10 or

Genus Rhopalonia Leger. Epimerite

more

digitiform processes; pseudocysts; spores cylindrical.

R. hispida (Schneider) (Fig. 235, /, g). Endoplasm yellowish orange; cysts 200-250// in diameter; spores 16m by 6.5/*; in gut of Geophiles sp. and Stigmatogaster gracilis.

Genus Dendrorhynchus

Keilin. Elongate; epimerite a disc, surfibrils

rounded by numerous ramified papillae; transverse

ous; cysts elliptical; spores fusiform.

conspicu-

D. system K. (Fig. 235, h). Sporadins 255m by 18.5-20^; spores 18-19m by In) in midgut of larvae of Systenus sp., a dolichopodid fly, found in decomposed sap of elm tree. Genus Trichorhynchus Schneider. Protomerite prolonged anteriorly into a long neck, dilated at tip; pseudocyst; spores cylindrical
to ellipsoidal.

T. pulcher S. (Fig. 235, i). Cysts 303-3 16m in diameter; spores 9.7m by 5.8m; in gut of Scutigera sp. and S. forceps (Watson, 1916). Genus Nina Grebnecki (Pterocephalus Schneider). Protomerite

made up
spirally at

of 2 long

narrow horizontal lobes fused and upturned one end, peripheral portion with many teeth, from which

project long filaments; spores in chain; in gut of myriapods. Species

(Fig. 235, j, k). 1.5-5 mm. long; cyst spherical; spores ellipsoidal in the gut of Scolopendra cingulata and S. subspini;

(Watson, 1916). N. gracilis G.

pes (Goodrich, 1938).

Genus Seticephalus Kamm. Protomerite with

like bristles.

closely set brush-

S. elegans (Pinto) (Fig. 235, I). Sporadins up to 75m by 35m; cysts and spores unknown; in gut of Scolopendra sp. Genus Acutispora Crawley. Solitary; pseudocyst; spore biconical,

SPOROZOA, GREGARINIDA

551

with a thick blunt endosporal rod at each end. One species (Crawley,
1903).

A. macrocephala C. (Fig. 235,

ra).

Sporadins up to 600^ long; cysts

spherical, 410/* in diameter; spores navicular, slightly curved, 19/z

by

4ju;

in

gut of Lithobius forficatus.

Fig. 235. a, b, Menospora polyacantha (Leger); c, d, Dactylophorus robustus (c, X130; d, X900) (Leger); e, Echinomera magalhaesi, X130 (Pinto); f, g, Rhopalonia hispida (g, X830) (Leger); h, Bendrorhynchus
systeni,

X770
(j,

(Keilin);

i,

Trichorhynchus pulcher (Schneider);

1,

j,

k,

Nina

gracilis

X10) (Schneider);
o, p,

Seticephalus elegans,
n,

X450

(Pinto);
schubergi,

m, Acutispora macrocephala,

X65 (Crawley);

Metamera

X270 (Duke); non and Ray); and Ray).

q, r,

Hentschelia thalassemae (o, X230; p, X620) (MackinLecythion thalassemae (q, X270; r, X930) (Mackinnon

552

PROTOZOOLOGY

Genus Metamera Duke. Epimerite eccentric, bordered with many branched digitiform processes; cysts without ducts; spores
biconical (Duke, 1910).

M.

by 7m;

schubergi D. (Fig. 235, n). Sporadins 150m by 45m; spores 9m in gut of the leeches, Glossosiphonia complanata and Placobreynoldsi Jones. Sporadins with epimerite

della marginata.

M.

measure 280m by

50m; cysts spherical; dehiscence by rupture; spore biconical, 5m by 3m, with 8 sporozoites; in the stomach diverticula and intestine of

Glossosiphonia complanata.

Genus Hentschelia Mackinnon and Ray. Epimerite with a short its margin divided into 4-5 lobes, each fluted on anterior surface; 2 sporadins encyst together; gametes anisogamous; flagellate and non-flagellate; zygote gives rise to a spherical spore with 8 sporozoites. One species. H. thalassemae M. and R. (Fig. 235, o, p). Cephalins 75-98m by 30-45m", in gut of Thalassema neptuni (Mackinnon and Ray, 1931). Genus Lecythion Mackinnon and Ray. Epimerite a low cone, surrounded by 14-15 petal -shaped lobes, with a neck; cysts and spores unknown. L. thalassemae M. and R. (Fig. 235, q. r). Cephalins 135m by 52m;
neck, umbrella-like with

epimerite about 27m long; in gut of Thalassema neptuni.

Family 10 Stylocephalidae

Ellis

Sporadins solitary; epimerite varied; pseudocysts; hat-shaped

spores in chains.

Genus Stylocephalus

Ellis.

Epimerite nipple-like; cysts covered

with papillae; in arthropods and molluscs. S. giganteus E. (Fig. 236, a). Sporadins 1.2-1.8
spherical,

mm.
sp.

long; cysts

450m

in diameter; spores subspherical black, 11m

by

7m;

in Eleodes sp.,
(Ellis, 1912).

Asida opaca, A.

sp.,

and Eusattus

(Coleoptera)

Genus Bulbocephalus Watson. Epimerite a

in

dilated papilla located

middle of a long neck( Watson, 1916a). B. elongatus W. (Fig. 236, b). Sporadins up to 1.6 mm. by 50m; nucleus diagonal; cysts and spores unknown; in gut of Cucujus larva
(acoleopteran).

Genus Sphaerorhynchus Labbe. Epimerite a small sphere

of a long neck.
S.

at end

ophioides (Schneider). Cephalins 1.3

long; terminal part 8.5m; sporadins 3-4

mm. long; mm. long; in

epimerite 220m gut of Acis sp.

SPOROZOA, GREGARINIDA
Genus Cystocephalus Schneider. Epimerite a
papilla with a short neck; spore hat-shaped.
C. algerianus S. (Fig. 236,
c,

553
large lance-shaped

d).

Sporadins 3-4

mm.

long; spores

10-10. 5/x long; in gut of Pimelia sp. (Labb6, 1899).

elongatus,

Stylocephalus giganteus, X65 (Ellis); b, Bulbocephalus c, d, Cystocephalus algeriamis (c, X6; d, X930) (Schneider); e, Lophocephalus insignis (Schneider); f, Acanthospora polymorpha, X1670 (L6ger); g, h, Corycella armata (h, X860) (Lger); i,
Fig. 236.
a,

Xl5 (Watson);

Prismatospora evansi, X50 (Ellis); j, k, Ancyrophora gracilis (k, X1250) (L6ger); 1, m, Cometoides capitatus (m, X1330) (L6ger); n, o, Actinocephahis acutispora (L6ger); p. Amphoroides calverti, X130 (Watson); q, Asterophora philica, X65 (Leidy); r, Steinina rotunda, X130 (Watson); s, Pileocephalus striatus, X 180 (Leger and Duboscq) t, Stylocystis praecox,
;

XSO

(L6ger).

Genus Lophocephalus Labbe. Epimerite sessile crateriform disc with crenulate periphery, surrounded by digitiform processes.
L. insignis (Schneider) (Fig. 236,
e).

Sporadins

mm.

long; cysts

rounded; 430/x by Helops striatus.

330/u;

pseudocysts; spores 10^ long; in gut of

554

PROTOZOOLOGY
Family 11 Acanthosporidae Leger

Sporadins solitary; epimerite

complex; cysts without sporoducts;

conical knob; spores

spores with equatorial and polar spines.

Genus Acanthospora Leger. Epimerite simple

with spines. A. polymorpha L. (Fig. 236, /). Sporadins polymorphic; up to 1 mm. long; protomerite cylindro-conical; deutomerite ovoidal; endo-

plasm yellowish brown; cyst 500-700m in diameter; spore with 4

spines at each pole and 6 at equatorial plane, 8m
of

by

4.4m; in gut

Hydrous ceraboides. Genus Corycella Leger. Epimerite globular, with 8 hooks; spores biconical, with one row of polar spines (Leger, 1892).
C. armata L. (Fig. 236,
g,

h).

Sporadins 280-300/x long; cysts

spherical, 250m in diameter; spores 13m

by

6.5m; in gut of larva of

Gyrinus natator. Genus Prismatospora

pole.

Ellis. Epimerite subglobular with 8 lateral hooks; spores hexagonal, prismatic with one row of spines at each

P. evansi E. (Fig. 236,

i).

Sporadins broadly conical, 400m long;

cysts 370m in diameter; without sporoducts; spores with 6 long spines at each pole, 1 1/x by 5.8m ; in gut of Tramea lacerta and Sym-

petrum rubicundulum; Michigan. Genus Ancyrophora Leger. Epimerite globular with 5-10 digitiform processes directed posteriorly; spores biconical, with spines. A. gracilis L. (Fig. 236, j, k). Sporadins 20G>-2 mm. long; cysts spherical, 200m in diameter; spores hexagonal in optical section, with 4 polar and 6 equatorial spines, 8.5m by 5m; in gut of larvae and adults of Carabus auratus, C. violaceus, C. sp., and of larvae of Silpha
thoracica (Coleoptera) (Leger, 1892).

filaments; spores with polar spines

I,

Genus Cometoides Labbe. Epimerite globular with 6-15 long and 2 rows of equatorial spines. m). Sporadins up to 2 mm. long, C. capitatus (Leger) (Fig. 236,

active; epimerite with 12-15 filaments, 32-35/* long; cysts

30%

in

diameter; spores 5.1m by 2.5/*; in gut of larvae of Hydrous sp. (Coleoptera) (Watson, 1916).

Family 12 Actinocephalidae Leger

Sporadins solitary; epimerite variously formed; cysts without sporoducts; spores irregular, biconical or cylindro-biconical; in gut
of insects.

Genus Actinocephalus

Stein.

Epimerite

sessile

or with a short

SPOROZOA, GREGARINIDA
neck, with 8-10 simple digitiform processes at
conical.
its

555

apex; spores bi-

A. acutispora Leger (Fig. 236,

cysts ovoid, 550-600/*
4.5/z

n, o).

Sporadins 1-1.5

mm.

long;

by 280/*; spores, acutely pointed, of 2 sizes, by 2.8^ and 6.4/* by 3.6/*; in gut of the coleopteran Silpha

laevigata.

112/* in

A. parvus Wellmer. Sporadins 180/* by 50/*; cysts rounded, 62diameter; spores spindle-form, 6-7.5/* by 3-3. 8/*; 8 diploid
first

chromosomes; the
f elder,

division in the zygote

is

meiotic; in the gut

of larvae of dog-flea, Ctenocephalus cams.

Development (Weschensessile papilla;

1938).

Genus Amphoroides Labbe. Epimerite a globular

protomerite cup-shaped; spores curved; in myriapods.

A.

calverti

cysts spherical, 380/* in diameter; spores

lactarius.

(Crawley) (Fig. 236, p). Sporadins up to 1670/* by 120/*; unknown; in gut of Callipus
disc with

Genus Asterophora Leger. Epimerite a thick horizontal

drobiconical; in Neuroptera and Coleoptera.
cysts

a milled border and a stout style projecting from center; spore cylin-

A. philica (Leidy) (Fig. 236, q). Sporadins 300/*-2 mm. long; and spores unknown; in gut of Nyctobates pennsylvanica (CrawSolitary; epimerite a short

ley, 1903).

Genus Steinina Lger and Duboscq.

biconical; in Coleoptera (Leger
S. rotunda
of

motile digitiform process, changing into a flattened structure; spore

and Duboscq, 1904).

Sporadins 180-250/* long;
in

Watson

(Fig. 236, r).

gut

Amara

augustata (Coleoptera) (Watson, 1915).

Genus Pileocephalus Schneider. Epimerite lance-shaped, with a

short neck.

P. striatus Leger and

ter a

Duboscq

(Fig. 236, s).

Sporadins

150/* long;

nucleus in protomerite; cysts spherical; in gut of larvae of Pty'diopcontaminata.

Stylocystis Leger. Epimerite a sharply pointed, curved

Genus

process; spores biconical (Leger, 1899).

S. praecox L. (Fig. 236,
200/* long; spores
t).

Sporadins up to 500/* long; cysts ovoidal,

papilla

Tanypus sp. Genus Discorhynchus Labbe. Epimerite a large spheroidal with collar and short neck; spores biconical, slightly curved.
8m by
5/*

in gut of larval

D. truncatus (Leger) (Fig. 237,

a, b).

Sporadins 300/* long; cysts

large flattened fluted

spherical, 140/x in diameter; in gut of larvae of Sericostoma sp.

Genus Anthorhynchus Labbe. Epimerite a

disc; spores biconical,

chained laterally.

556

PROTOZOOLOGY

c, d). Cephalins up to 2 mm. long, with 200m long epimerite; protomerite 150m long; endoplasm opaque; spores 7ju by 5m; in gut of Phalangium opilio.

A. sophiae (Schneider) (Fig. 237,

Genus Sciadiophora Labbe. Epimerite a

spores biconical.

large sessile disc with

crenulate border; protomerite with numerous vertical laminations;

Fig. 237. a, b, Discorhynchus truncatus (a, X130) (Leger); c, d, Anthorhynchus sophiae (c, Xl5; d, X1330) (Schneider); e-g, Sciadiophora phalangii (g, spore, X1040) (L6ger); h, Amphorocephalus amphorellus (Ellis); i, Pyxinia bulbifera (Watson); j, Schneideria mucronata, X75 (Lger); k, Beloides firmus (L6ger); 1, Taeniocystis mira, X85 (L6ger); m, n, Stictospora provincialis (Ledger); o, Bothriopsis histrio (L6ger); p-r, Coleorhynchus heros (p, Xl4) (Schneider); s, Legeria agilis (Schneider); t-v, Phialoides ornata (t, X45; v, X930) (L6ger); w, Geneiorhynchus aeschnae, X60 (Crawley). S. phalangii (Leger) (Fig. 237, e-g). Sporadins 2-2.5

mm.

long;

protomerite with 15-16 plates; cysts 500m in diameter; spores 9m by 5^; in gut of Phalangium crassum and P. cornutum (Arachnida).
fluted disc set
ficially;

Genus Amphorocephalus Ellis. Epimerite a sessile peripherally upon a short neck; protomerite constricted superspores

unknown

(Ellis, 1913).

SPOROZOA, GREGARINIDA
A. amphorellus E. (Fig. 237,
of Scolopendra heros.
h).

557

Sporadins 500-970/* long; in gut

crateri-

Genus Pyxinia Hammerschmidt. Epimerite a crenulate

form
disc;

with a style in center; spores biconical. Species (Vincent,

1922).

in

Watson (Fig. 237, i). Sporadins up to 850m by 260m; gut of Dermestes lardarius (Watson, 1916a). Genus Schneideria Leger. Epimerite sessile, a thick horizontal
P. bulbifera

disc with milled border; a style arising

from center; sporadins with-

out protomerite; spores biconical (Leger, 1892).

S. mucronata L. (Fig. 237, j). Sporadins 700-800m long; agile; polymorphic; cysts 270m by 190m; spores fusiform, 15m by 9m; in

intestinal caeca of larvae of Bibio marci.

Genus Beloides Labbe. Epimerite bordered by pointed

processes and apical style; spores biconical (Labbe, 1899).

lateral

B. firmus (Leger) (Fig. 237,

in diameter; spores 14. 5m

k).

Style 80m long; cysts 180-200m

by

6m; in gut of larvae of Dermestes lar-

darius.

Genus Taeniocystis Leger. Epimerite sessile or with a short neck; 8-10 digitiform processes at its apex; deutomerite divided by septa into many chambers; spores biconical. T. mira L. (Fig. 237, I). Sporadins tapeworm-like; 400-500m long; epimerite with 6-8 curved hooks; cysts spherical, 130m in diameter; spores 7m by 3m; in gut of larval Ceratopogon solstitialis.

Genus Stictospora Leger. Epimerite with a short neck, a spherical

crateriform ball with 12 posteriorly-directed laminations set

close to neck; cysts with a gelatinous envelope; without ducts;

spores biconical, slightly curved (Leger, 1893).

S. provincialis L. (Fig. 237, m, n). Sporadins 1-2 mm. long; cysts 800m in diameter; in gut of larvae of Melolontha sp. and Rhizotrogus
sp.

Genus Bothriopsis Schneider. Epimerite sessile, small, oval, with 6 or more filamentous processes directed upward; spores biconical;
cysts spherical (Schneider, 1875).

B. histrio S. (Fig. 237,

sp.

o).

long; cysts 400-500m long; spores 7.2m

Epimerite with 6 filaments, 80-90m by 5m; in gut of Hydaticus

discoid,

Genus Coleorhynchus Labbe. Epimerite

over deutomerite; spores biconical.

lower border

C. heros (Schneider) (Figs. 234, k; 237, p-r). Sporadins 2-3

mm.
epi-

long; in gut of

Nepa

cinerea.

Development (Poisson,

1939).

Genus Legeria Labbe. Protomerite wider than deutomerite;

558

PROTOZOOLOGY
cysts

merite unknown;

without duct; spores cylindro-biconical

s).

(Labbe, 1899).
L. agilis (Schneider) (Fig. 237,
betes sp.

In gut of the larvae of Colym-

Genus Phialoides Labbe. Epimerite a cushion set peripherally with stout teeth, surrounded by a wider collar; with a long neck; cysts spherical, without ducts; spores biconical.
P. ornata (Leger) (Fig. 237,
t-v).

300-400/x in diameter; spores 10.5/t

by

Sporadins 500/* long; cysts 6.7/*; in gut of larvae of

tuft

Hydrophilus piceus.

Genus Geneiorhynchus Schneider. Epimerite a

end of neck; spores cylindrical. G. aeschnae Crawley (Fig. 237, w). Sporadins and spores unknown; in Aeschna constricta.
bristles at

of short

420// long; cysts

Family 13 Porosporidae Labbe

When naked
and midgut of a
ed

or well-protected sporozoites enter the stomach

specific crustacean host,
1,

they develop into typi-

cal cephaline gregarines;

2,

or more sporadins become associat-

and encyst. Repeated nuclear and cytoplasmic division reformation of an enormous number of gymnospores in hindgut. Some observers consider this change as schizogony, and hence
sults in

include the family in the suborder Schizogregarinina.

When

the
in

gymnospores are voided

in the faeces of crustaceans

and come

contact with molluscan host, they enter, or are taken in

by phago-

cytosis of, the epithelial cells of the gills, mantle or digestive system. These gymnospores are found especially in abundance in the lacunae of the gills. Presently they become paired and fuse (Hatt) the zygotes develop into naked or encapsulated sporozoites within the phagocytes of the molluscan host, which when taken in by a

crustacean host, develop into cephaline gregarines.

Genus Porospora Schneider. Sporozoites formed in molluscan phagocytes without any protective envelope (Hatt, 1931). P. gigantea (van Beneden) (Fig. 238, a-f). Sporadins in Homarus gammarus, up to 10 mm. long; cysts 3-4 mm. in diameter; gymnospores spherical, 8/i in diameter (Hatt), containing some 1500 merozoites; in molluscan hosts, Mytilus minimus and Trochocochka mutabilis, they develop into naked sporozoites (17/* long) which are usually grouped within phagocytes.
Genus Nematopsis Schneider. Development similar
to that of

Porospora (Hatt); but each sporozoite in a double envelope. N. legeri (de Beauchamp) {Porospora galloprovincialis L6ger and

SPOROZOA, GREGARINIDA
f

559

Fig. 238. a-f, Porospora gigantea (Hatt). a, a cephalin attached to gut, X1250; b, gymnospores; c, d, developing sporozoites in mollusc; e, sporozoites enveloped by phagocyte; f, a sporozoite, X2250. g-n, Nematopsis legeri (Hatt). g, h, trophozoites in Eriphia; associated trophozoites attached to gut-epithelium, X1250; j, gymi, nospores ;k, gymnospores after entering molluscanbody; 1, a young sporozoite, X2250; m, cyst in mollusc with six spores; n, germination of a

Homarus

spore in Eriphia gut, X1250.

frons, in linear or bifurcated

Sporadins in a crustacean, Eriphia spinisyzygy 75-7 50 m long; cysts about 80 m in diameter; gymnospores 7/x in diameter, composed of fewer, but larger merozoites; permanent spores with a distinct one-piece shell (endospore) and a less conspicuous epispore, about 14-15ju long and circular in cross-section, develop in numerous species of molluscan

Duboscq)

(Fig. 238, g-n).

560

PROTOZOOLOGY
M. minimus, Lasea
rubra, Cardita

hosts: Mytilus galloprovincialis,

calyculata, Chiton caprearum, Trochocochlea turbinata, T. articulata,

T. mutabilis, Phorcus richardi, Gibbula divaricata, G. rarilineata, G. adamsoni, Pisania maculosa, Cerithium rupestre, ColumbcUa rustica, and Conus mediterraneus in European waters (Hatt, 1931).

N. ostrearum Prytherch. Sporadins in syzygy in the mud crabs, Panopeus herbsti and Eurypanopeus depressus, 220-342 n; cysts 80190^ in diameter; gymnospores 4/* in diameter; spores produced in the oyster, Ostrea virginica, 16^ by 11-12/z (Prytherch, 1940). Landau and Galtsoff (1951) showed that the organism is widely distributed among the oysters along the Atlantic and Gulf coasts, but found no evidence to suppose that the organism is destructive to the
host mollusc.

N. panopei

Ball.

Sporadins up to 210/x by

14/z;

protomerite about

1/15 the body length; epimerite on young individuals only; syzygy often multiple, as in other species; cysts 88 ^ by 74^, free in the lumen or attached to the wall of the hind-gut; gymnospores about
6.5^ in diameter; in the gut of Panopeus herbsti and P. occidentalis
in

Bermuda. Molluscan host unknown

(Ball, 1951).

Suborder 2 Schizogregarinina Leger

The
nelids,

schizogregarines are intestinal parasites of arthropods, an-

and tunicates.

When

the spore gains entrance to the diit

gestive tract of a specific host through mouth,

into trophozoites either in the

germinates and

the sporozoites are set free (Fig. 239). These sporozoites develop

gut-lumen or within the host cells, which may be binary or multiple fission or budding. The fully grown trophozoites become paired as in Eugregarinina and encyst, in which condition they undergo sexual reproduction. Each individual which is now a gametocyte produces gametes (d-e). Fusion of two gametes follows (/). The

and undergo schizogony

(c),

zygote develops into a spore containing 1-8 sporozoites

(g, a).

One spore from 2 gametocytes Two or more spores from 2 gametocytes

Family

Ophryocystidae
(p.

Family 2 Schizocystidae

562)

Family

Ophryocystidae Leger and Duboscq

in

Two

gametocytes produce one spore;

Malpighian tubules of
or mul-

Coleoptera, gut of Ascidia and coelom of Oligochaeta.

Genus Ophryocystis Schneider. Multiplication by binary

tiple division; extracellular; trophozoites conical,
cells

attached to host

by pseudopods; a

single spore in a pair of spheroidal

gameto-

SPOROZOA, GREGARINIDA

561

Fig. 239.
a,

The

life-cycle of Schizocystis gregarinoides,

X1000

(Leger).

germinating spore; b, growth of schizonts; c, schizogony; d, two gametocytes and their association; e, stages in gamete formation, f, zygote formation, g, cyst containing zygotes, each of which develops into
a spore

shown in

a.

cytes; spore with 8 sporozoites; in Malpighian tubules of Coleoptera. Several species.

0. mesnili Leger (Fig. 240, a-e). In Tenebrio molitor; schizonts 1-4 nuclei; gametocytes llju in diameter; pairs 16-17^ by 11/x;
llju by 7/z. Genus Merogregarina Porter. Schizogony intracellular; trophozoites attached to gut epithelium by a proboscidiform organel-

spores biconical,

la;

2 gametocytes giving
sp.;

rise to
/,

one spore containing 8 sporozoites.

g).

M. amaroucii
roucium

P. (Fig. 240,

In gut of the ascidian,

Ama27-31yu

extracellular;

trophozoites with epimerite,

long; spore about 14/x long.

a(32

Fig. 240. a-e, Ophryocystis mesnili (a, trophozoite attached to Malpighian tubule; b-e, sporogony), X1330 (Leger); f, g, Merogregarina amaroucii, X1000 (Porter); h, i, Spirocystis nidula (h, X770; i, X500) (L6ger and Duboscq); j, k, Caulleryella pipientis (j, gut of Culex pipiens with trophozoites, X200; k, a spore, X1200) (Buschkiel).

Genus Spirocystis Leger and Duboscq. Schizogony intracellular; curved, one end highly narrowed; mature schizonts snail-like, with numerous nuclei; repeated schizogony (?); gametes in chloragogen cells, somatic and visceral peritonium; association
schizonts

gametes produces a spore. One species. and D. (Fig. 240, h, i). In coelom and gut epithelium of Lumbricus variegatus; multinucleate schizont about 35/z long; microgametes fusiform or ovoid, 7/x by 3/x| macrogametes ovoid or spherical, 11/x in diameter; fusion of 2 gametes produces one spore which is thick-walled, 35/x long and contains one sporozoite, up to 40^ long.
of 2
S. nidula L.

Family 2 Schizocystidae Leger and Duboscq

Two

or more spores are produced in a pair of gametocytes. Genus Schizocystis Leger. Mature trophozoite multinucleate;

ovoid or cylindrical with differentiated anterior end; schizogony

by multiple division; trophozoites become associated, encyst, and produce numerous (up to 30) spores, each with 8 sporozoites; in Diptera, Annelida, and Sipunculoida (Leger, 1909).
S. gregarinoides L. (Fig. 239). In

gut of larvae of Ceratopogon

SPOROZOA, GREGARINIDA
solstitialis;

563

coiled;

mature schizonts up to 400/z by 15m; curved or spirally gametocytes 30-50/z long; cysts ovoid, 16-32ju long; spores

S/x by 4m. Genus Syncystis Schneider. Schizogony and sporogony extracellular; young trophozoites elongate, amoeboid; mature schizonts more or less spheroidal, producing some 150 merozoites; cysts spherical, producing about 150 spores. One species. S. mirabilis S. (Fig. 241, k, I). In coelomic fluid and fat bodies of Nepa cinerea; merozoites, In long; cysts spherical; spores navicular, 3-4 spines at ends, 10m by 6m, with 8 sporozoites. Genus Mattesia Naville. Schizogony in the adipose tissue cell; 2 spores produced by a pair of gametocytes. One species. Meiosis

biconical,

(Naville, 1930).

M.

dispora N. (Fig. 241, m). In adipose tissue cells of larvae of

also); schizonts 2.5-12/x long;

the flour moth, Ephestia kuhniella and Plodia interpunctella (pupa

and adult
ville,

cyst 8-12/x in diameter,

with 2 spores, each with 8 sporozoites; spores 14m by 7.5m (Na1938); 11m by 6m (maximum 13.5m by 8m) (Musgrave and Mackinnon). Highly pathogenic according to Musgrave and Mackinnon. Genus Caulleryella Keilin. Multiplication extracellular; each

gametocyte gives
species.

rise to

8 gametes, a pair forming 8 zygotes or

spores; spore with 8 sporozoites; in gut of dipterous larvae. Several

C. pipientis Buschkiel (Fig. 240, j, k). Average trophozoites 50-60m by 23-26m; with paraglycogen grains; schizogony produces 30-38 merozoites; in gut of larvae of Culex pipiens. Genus Lipotropha Keilin. Schizogony and sporogony intracellular; cyst contains 16 spores, each with 8 sporozoites; in fat body of Systenus larvae. One species. L. macrospora K. (Fig. 241, n). Spores about 13.5m by 3mGenus Lipocystis Grell. Schizogony and sporogony intracellular; gamete formation on the surface of cytomeres; isogamy; cyst produces 100-200 spores, each with eight sporozoites. One species (Grell,

1938).

L. polyspora G. (Fig. 242, a). Spores elongate ellipsoid, about 10m

by 4m; in the fat body of Panorpa communis. Genus Selenidium Giard. Schizogony intracellular; many spores produced by a pair of extracellular gametocytes; spore with 4 or more sporozoites; in gut of annelids. Generic status (Mackinnon and
Ray, 1933).
S. potamillae

euglenoid, average size 40m

Mackinnon and Ray by 15m;

(Fig. 241, a-c).

Trophozoites

longitudinal striae; cysts ob-

564
long, producing

PROTOZOOLOGY
many
spores; spore, spherical with 4 (up to 10)

sporozoites; in gut of the polychaete, Potamilla reniformis (Mackin-

non and Ray, 1933). Genus Meroselenidium Mackinnon and Ray. Schizogony intracellular, initiated by formation of small masses which give rise

Fig. 241. a-c, Selenidium potamillae (a, X420; b, cyst with spores, (Mackinnon and Ray); d-f, Meroselenidium keilini c, spore) (d, sporadin, X670; e, f, different views of spore, X930) (Mackinnon and Ray); g-j, Machadoella triatomae (g, a schizont, X1420; h, i, a single and associated sporadins, X710; j, spore, X1920) (Reichenow); k, 1, Syncystis mirabilis: k, a cyst, X470 (Steopoe); 1, spore (Schneider); m, Mattesia dispora, X1480 (Naville); n, Lipotropha macrospora, X800

X330;

(Keilin).

about 20 spores from a pair of gametocytes; spores with numerous sporozoites. One species (Mackinnon and Ray, 1933).
to merozoites;

M.
by

keilini

30/x;

M. and R. (Fig. 241, d-f). Large schizonts about 150/x sporadins free in gut 200-300^ by 40-70^; paired gametoby
40jli;

cytes 85/x

verse ridges, with

many

spores 26-28m by 14-16/x, bivalve (?), transsporozoites; in gut of Potomilla reniformis.

leaf -like

Genus Selenocystis Dibb. Sporadins

with a median ridge;

biassociation with posterior ends, forming an elongated cyst, at-

SPOROZOA, GREGARINIDA
tached to the host epithelium
species (Dibb, 1938).

565

by a

foot-like organelle; isogametes

with a short flagellum; spores with four or eight sporozoites. One

(Ray) (Fig. 242, b-f). Trophozoites 30-250 /x long; pelwith 16-24 striae; the broader end with which the organism is attached to the host epithelium depressed surrounding this depression, a number of about 8/i long refringent filaments occur; while one
S. foliata
licle
;

v.,^r*T.>---

Fig. 242.

a,

two views

of

a spore

of

Lipocystis polyspora,

X1485

mature trophozoite, X665 (Ray); c, migration of nuclei of gametocytes to the surface of cyst, X565; d, gamete in life; e, f, spores with four and eight sporozoites, X1130 (Dibb)).
(Grell); b-f, Selenocystis foliata (b, a

organism
in

is

still

attached, biassociation by posterior ends takes

place; 26-226/x

9-34/*; isogametes; subspherical spores about 8.5m diameter, with four or eight sporozoites; in the gut of the poly-

by

chaete, Scolelepis fuliginosa.

Genus Machadoella Reichenow. Nematode-like, rigid; simple rounded anterior end; thick pellicle, longitudinally striated; schizogony in vermiform stage; head to head association of gametocytes; cysts with 3-6 spores, each with 8 sporozoites. M. triatomae R. (Fig. 241, g-j). Schizonts about 55/x long; gametocytes 100-120/x long; schizogony into 6-8 merozoites; cysts with 3-6 spores; spore 10-1 1/x by 7-7. 5^; in Malpighian tubules of Triatoma dimidiata (of Guatemala) (Reichenow, 1935).
References

Doflein, F. and Reichenow, E.: (1929) Lehrbuch der Protozoenkunde. 5 ed. Jena.

Labbe, A.: (1899) Sporozoa. In: Das Tierreich. Part Naville, A.: (1931) Les Sporozoaires. M6m d.'hist.
41:1.
:

5.

nat.,

Geneva,

Reichenow, E. (1932) Sporozoa. Grimpe's Die Tierwelt der Nordund Ostsee. 21 pt. 2-g.
:

566

PROTOZOOLOGY
F.: (1900) Untersuchungen ueber Generationswechsel bei Coccidien. Zool. Jahrb. Anat., 13: 197.

Schaudinn,

Wenyon,
Adams,

C. M.: (1926) Protozoology.

:

1, 2.

London and Baltimore.

J. A. and Travis, B. V. (1935) Two new species of gregarine Protozoa from the firebrat, etc. J. Parasit., 21:56. Allegre, C. F. (1948) Contributions to the life history of a gregarine parasitic in grasshoppers. Tr. Am. Micr. Soc, 67:211. Ball, G. H.: (1938) The life history of Carcinoecetes hesperus, etc. Arch. Protist., 90:299. (1951) Gregarines from Bermuda marine crustaceans. Univ. California Publ. Zool, 47:351. Berlin, H.: (1924) Untersuchungen ueber Monocystideen in den Vesiculae seminales der schwedischen Oligochaeten. Arch.
:

Protist., 48:1.

Bhatia, B.

L.: (1929) On the distribution of gregarines in oligochaeParasitology, 21 120. (1930) Synopsis of the genera and classification of haplocyte gregarines. Ibid., 22:156. and Chatterjee, G. B.: (1925) On some gregarine parasites of Indian earthworms. Arch. Protist., 52:189. and Setna, S. B.: (1926) On some more gregarine parasites of Indian earthworms. Ibid., 53:361. Buschkiel, Marianne: (1921) Caulleryella pipientis, etc. Zool. Jahrb. Anat., 43:97. Calkins, G. N. and Bowling, R. C: (1926) Gametic meiosis in Monocystis. Biol. Bull., 51:385. Chakravarty, M.: (1935) Studies on Sporozoa from Indian millipede. IV. Arch. Protist., 86:211. (1936) V. Ibid., 88:116. Crawley, H.: (1903) List of polycystid gregarines of the United States. Proc. Acad. Nat. Sc. Philadelphia, 55:41. (1903a) II. Ibid., 55:632. - (1907) III. Ibid., 59:220. Dibb, M. J.: (1938) Selenocystis foliata (Ray) from Scolelepis fuliginosa, and its identity with Haplozoon sp. Parasitology, 30:296. Duke, H. L.: (1910) Some observations on a new gregarine (Metamera schubergi n.g., n. sp.). Quart. J. Micr. Sc, 55:261. new species of polycystid gregarine from the Ellis, M. M.: (1912) United States. Zool. Anz., 39:25. descriptive list of the cephaline gregarines of the (1913) New World. Tr. Am. Micr. Soc, 32:259. (1913a) New gregarines from the United States. Zool. Anz., 41:462. (1914) An acanthosporid gregarine from North American dragonfly nymphs. Tr. Am. Micr. Soc, 33:215. Gates, G. E.: (1933) On a new gregarine from the coelom of a Burmese earthworm, Pheretima compta. Biol. Bull., 65:508. Gohre, E.: (1943) Untersuchungen ueber den plasmatischen Feinbau der Gregarinen, etc. Arch. Protist., 96:295.

tes.

SPOROZOA, GREGARINIDA
Goodrich, E.
S.

567

P.: (1920) Gonospora Quart. J. Micr. Sc, 65: 157. Goodrich, Helen P.: (1925) Observations on the gregarines of Chiridota. Ibid., 69:619. (1938) Nina: a remarkable gregarine. Ibid., 81:107. (1949) Heliospora n.g. and Rotundula n.g., etc. Ibid., 90:

and Goodrich, Helen L. M.

minchini, n.

sp., etc.

27.

- (1950) Sporozoa of Sipunculus. Ibid., 91:469. Grell, K. G.: (1938) Untersuchungen an Schizogregarinen.
Arch. zool. exper. gen., 72:341.

I.

Arch.

Protist., 91: 526. Hatt, P.: (1931) L'evolution des porosporides chez les mollusques.

Hesse, E.: (1909) Contribution a l'etude des monocystidees des

Jameson, A.

Oligochaetes. Ibid., 3:27. P.: (1920) The chromosome cycle of gregarines, with special reference to Diplocystis schneideri. Quart. J. Micr. Sc, 64:207. Jones, A. W. (1943) Metamera reynoldsi n. sp., etc. Tr. Am. Micr. Soc. 62:254. Kamm, Minnie W.: (1920) The development of gregarines and their relation to the host tissues. III. J. Parasit., 7:23. (1922) Studies on gregarines. II. Illinois Biol. Monogr., 7:1. (1922a) A list of the new gregarines described from 1911 to 1920. Tr. Am. Micr. Soc, 41:122. Keilin, D.: (1920) On two new gregarines, etc. Parasitology, 12:
:

154.

Landau, Helen and Galtsoff,

topsis infection

P. S.: (1951) Distribution of

Nema-

and Leger,

in

on the oyster grounds of the Chesapeake Bay other waters of the Atlantic and Gulf states. Texas J. Sc,

3:115.
L.: (1892) Recherches sur les gregarines. Tabl. zool., 3:1. (1893) Sur une gregarine nouvelle des acridiens d'Algerie.

C. R. Acad. Sc, 117:811. (1906) Etude sur Tacniocystis mira Leger, etc. Arch. Protist., 7:307. (1907) Les schizogregarines des tracheites. I. Ibid., 8: 159. (1909) II. Ibid., 18:83. and Duboscq, O.: (1915) Etudes sur Spirocyslis nidula, etc Ibid., 35:199. (1925) Les porosporidies et leur evolution. Trav. St. zool. Wimereux, 9:126. Leidy, J.: (1853) On the organization of the genus Gregarina of Dufour. Tr. Am. Philos. Soc, n.s., 10:233. Mackinnon, Doris L. and Ray, H. N.: (1931) Observations on dicystid gregarines from marine worms. Quart. J. Micr. Sc, 74:439. (1933) The life cycle of two species of "Selenidium" from the polychaete worm Potamilla reniformis. Parasitology, 25:143. Martiis, L. Cognetti de: (1911) Contributo alia conoscenza delle

568

PROTOZOOLOGY
Monocistidee e dei loro fenomeni riproduttivi. Arch. Protist., 23:205. (1921) Resultats de l'expedition scientifique Neerlandaise a la Nouvelleguinee. XIII. Zoologie, 4:501. (1923) Sul genera Monoeystis. Monit. Zool. Ital. Firenze, 34:
250. (1925) Sulla classificazione e sui caratteri tassonomici delle Monocistidee degli oligocheti. Ibid., 36:219.

(1926) Due nuove Gregarine Monocistidee a miocito profondo. Boll. Musei Zool. e Anat. Com. Sec. Ser. 6:17. Mercier, L.: (1911) Cephaloidophora cuenoti n. sp., etc. C. R. soc. biol., 71:51. Muhl, Dorothea: (1921) Beitrag zur Kenntnis der Morphologie und Physiologie der Mehlwurmgregarinen. Arch. Protist., 43: 361. Mulsow, K.: (1911) Ueber Fortpflanzungserscheinungen bei Monoeystis rostrata n. sp. Ibid., 22:20. Musgrave, A. J. and MacKinnon, Doris L.: (1938) Infection of Plodia inter punctella with a schizogregarine, Mattesia dispora. Proc. Roy. Entom. Soc. London (A), 13:89. Naville, A.: (1930) Recherches cytologiques sur les schizogregarines. Ztschr. Zellf. mikr. Anat., 11:375. Noble, E. R.: (1938) The life-cycle of Zygosoma globosum sp. nov., a gregarine parasite of Urechis caupo. Univ. California Publ. Zool., 43:41. (1938a) A new gregarine from Urechis caupo. Tr. Am. Micr. Soc, 57:142. Pinto, C: (1918) Contribuicao as estudo das gregarines. Trav. Inst. Oswaldo Cruz, 113 pp. Poisson, R. (1939) A propos de Coleorhynchus heros, gregarine parasite de la Nepe cendree. Bull. biol. France et Belg., 73:275. Prytherch, H. F.: (1940) The life cycle and morphology of Nematopsis ostrearum, etc. J. Morphol., 66:39. Ray, H. N.: (1930) Studies on some Sporozoa in polychaete worms. I. Parasitology, 22:370. Reichenow, E.: (1935) Machadoella triatomae, etc. Arch. Protist., 84:431. Schiffmann, Olga (1919) Ueber die Fortpflanzung von Gregarina blattarum und G. cuneata. Ibid., 40:76. Schneider, A.: (1875) Contributions a l'histoire des gregarines des invertebres de Paris et de Roscoff. Arch. zool. exper., 4:493. Smith, L. M.: (1929) Coccospora stenopelmati, etc. Univ. California Publ. Zool., 33:57. (1930) Further observations on the protozoan Tettigonospora. Ibid., 33:445. Sprague, V.: (1941) Studies on Gregarina blattarum with particular reference to the chromosome cycle. Illinois Biol. Monogr., 18: no. 2. Troisi, R. L.: (1933) Studies on the acephaline gregarines of some oligochaete annelids. Tr. Am. Micr. Soc, 52:326.
:
:

SPOROZOA, GREGARINIDA
Vincent, Mary: (1922) On the life history Pyxinia anobii, etc. Parasitology, 14:299.
(1924) 16:44.
of a

569

new

gregarine:

On

new

gregarine Anisolobus dacnecola, etc. Ibid.,

Some new gregarine parasites from Ar2:27. (1916) Studies on gregarines. Illinois Biol. Monogr., 2:213. (1916a) Observations on polycystid gregarines from Arthropoda. J. Parasit., 3:65. Weschenfelder, R.: (1938) Die Entwicklung von Actinocephalus parvus. Arch. Protist., 91 1. Zwetkow, W. N.: (1926) Eine neue Gregarinengattung Enter ocystis ensis, etc. Arch. russ. protist., 5:45.
Watson, Minnie:
thropoda.
(1915)
J. Parasit.,
:

Chapter 25

Order 2 Coccidia Leuckart

Coccidia show a wide THE vertebrates and higher invertebrates
all

zoological distribution,
alike.

attacking
its asso-

The majority

are parasites of the epithelium of the digestive tract and

ciated glands. Asexual reproduction
is

reproduction

by anisogamy

in

of reproduction take place in

by schizogony and sexual the majority of species. Both kinds one and the same host body, with

the exception of such forms as Aggregata in which alternation of

generations and of hosts occurs.

Taxonomy

(Leger, 1911).

Gametocytes similar; independent; a microgametocyte developing into Suborder 1 Eimeridea many microgametes Gametocytes dissimilar; association begins during the late trophic life; Suborder 2 Adeleidea (p. 590) a few microgametes

Suborder

Eimeridia Leger

These coccidians are, as a rule, intracellular parasites of the gut epithelium. Both asexual (schizogonic) and sexual (sporogonic) generations occur in one host, although in some there is also alternation of hosts. The life-cycle of Eimeria schubergi, a gut parasite of the centipede, Lithobius forficatus, as observed by Schaudinn, is as follows (Fig. 243). The infection begins when the mature oocysts of the coccidian gain entrance into the host through the mouth. The sporozoites escape from the spores and make their way through the micropyle of the oocyst into the gut lumen (p). By active movement they reach and enter the epithelial cells (a). These schizonts grow into large rounded bodies and their nuclei multiply in number. The newly formed nuclei move to the body surface, and each becomes surrounded by a small mass of cytoplasm, forming a merozoite. When the host cells rupture, the merozoites are set free in the gut lumen, make their way into new host cells and repeat the development (6). Instead of growing into schizonts, some merozoites transform themselves into macro- or micro-gametocytes (c). Each macrogametocyte contains retractile bodies, and becomes a mature macrogamete, after extruding a part of its nuclear material (d, e). In the microgametocyte, the nucleus divides several times and each division-product assumes a compact appearance (f-h). The biflagellate comma-shaped microgametes thus produced, show activity when freed from the host cells (i). A microgamete and a macrogamete unite to form a zygote which secretes a membrane around itself (j). This stage is
570

COCCIDIA

571

243. The life-cycle of Eimeria schubergi, X-400 (Schaudinn) entrance of a sporozoite in the gut epithelial cell of host and growth of schizont; b, schizogony; c, macro- and micro-gametocyte; d, e, formation of macrogamete; f-h, formation of microgametes; i, mature gametes prior to fusion, j, k, fertilization; 1-n, spore-formation; o, oocyst containing four mature spores, each with two sporozoites; p, germination

Fig.

a,

of spores in host's gut.

and produces four becomes the center of a sporoblast which secretes a membrane and transforms itself into a spore (n). Its nucleus, in the meantime, undergoes a division, and two sporozoites develop in the spore (o). Oocysts leave the host in the faecal matter and become the source of infection.
as the oocyst.

known

The nucleus

divides twice

nuclei (k-m).

Each

of the four nuclei

Body vermiform; schizogony

Body not vermiform

in motile stage

Family
.

Selenococcidiidae

(p.

572)
572)

Alternation of generations and of hosts Family 2 Aggregatidae Only one host Gametocytes become associated early; many microgametes Family 3 Dobelliidae Family 4 Eimeriidae Gametocytes independent
.

(p.

(p.
(p.

576) 576)

572

PROTOZOOLOGY
Family
1

Selenococcidiidae Poche

Vermiform body and gametic differentiation place this family on the borderline between Coccidia and Gregarinida. Genus Selenococcidium Leger and Duboscq. Nucleus of vermiform trophozoite divides 3 times, producing 8 nuclei; trophozoite becomes rounded after entering gut-epithelium and divides into
8 schizonts; this
is apparently repeated; schizonts develop into gametocytes; microgametocyte produces numerous microgametes gametic union and sporogony (?). One species.

Fig. 244. Selenococcidium intermedium,

a,

X550 (Leger and Duboscq).

d,

schizont in host gut; b,

f,

c,
r

schizogony;

gametes;
S.

macrogametoc}

te; g,

microgametocyte; e, micromacrogamete; h, zygote (oocyst).

intermedium L. and D. (Fig. 244). Octonucleate vermiform

schizont 60-100m long, and divides into vermicular merozoites in

cells; parasitic in gut lumen of European lobster. Genus Ovivora Mackinnon and Ray. Trophozoites large and vermiform (Fig. 245, a) gametocytes spherical (c) large macrogametocytes; small microgametocytes, giving rise to numerous biflagellate

gut

microgametes

(d):

oocyst

membrane

delicate

or

lacking;

ovoid

number of sporozoites; schizogony produces many merozoites; one host. One species (Macspores contain variable (averaging
12?)

kinnon and Ray, 1937).

0. thalassemae (Lankester) (Fig. 245). In the egg of the echiurid

worm, Thalassema neptuni; merozoites about 10m long (b) macrogametocytes (c) 40-75^ in diameter; microgametocytes (c) 23-65/x; chromosome reduction, 14 to 7, in the zygote; spores (/) 15.5^ by 13.5/x (Mackinnon and Hay, 1937).
;

Family 2 Aggregatidae Labbe

Anisogamy
formed into

results in production of zygotes

which become trans-

many

spores, each with 2-30 sporozoites; in schizogony

COCCIDIA

573

cytomeres first appear and then merozoites; alternation of generations and of hosts which are marine annelids, molluscs and crustaceans.

Genus Aggregata Frenzel. Schizogony in a crustacean and sporogony in a cephalopod; zygote produces many spores, each with 3
sporozoites.

Many

species.

Cytology (Moroff, 1908).

organisms

Fig. 245. Ovivora thalassemae (Mackinnon and Ray)- a, two mature in host egg, seen in reflected light, X250; b, schizonts in sectioned egg; c, micro- and macro-gametocytes in an egg, X500; d, two
still

maturing microgametes
e,

cyst with zygotes in some of which nuclei are dividing, X500; with 10 nuclei, X900.

attached to cytoplasmic residuum, X1075; f, a spore

A. eberthi (Lab-be) (Fig. 246). Schizogony in Portunus depuraand sporogony in Sepia officinalis. Spores (a) germinate in the crab gut, each liberating 3 sporozoites (b) which grow and produce merozoites (10/x by 2/x) by schizogony in peri-intestinal connector

tive tissue cells (6

chromosomes)

(c-/);

when host crab

is

eaten by

a cuttlefish, merozoites penetrate gut wall and develop into mi-

and macro-gametocytes (h, k), and further into gametes (j-l); anisogamy (m) produces zygotes; zygote nucleus contains 12 chromosomes which become divided into 2 groups of 6 in the first
cro-

division (n, o); repeated nuclear division (p) forms many sporoblasts (q), each transforms itself into a spherical spore with 3 sporozoites (Dobell, 1925; Naville, 1925; Belaf, 1926).

574

PROTOZOOLOGY

Fig. 246. The life-cycle of Aggregata eberthi (Dobell). a, a mature spore; b, germination of spore; c-f, schizogony; g, a merozoite, swallowed by Sepia; h-j, development of microgametes; k-1, development of macrogamete; m, fertilization; n, o, first zygotic division, chromosomes reduced in number from 12 to 6; p, q, development of sporoblasts, each of

which develops into a spore with three sporozoites.

Genus Merocystis Dakin. Sporogony in the kidney of the whelk, Buccinum; schizogony unknown, in another host (possibly a crab); microgametocytes produce first C3^tomeres which in turn form microgametes; anisogamy gives rise to zygotes, zygote forms many
sporoblasts, each developing into a spore; spore spherical, with 2
sporozoites.

One species.

a, b). In the kidney of Buccinum undatum; spores spherical, about 14^ in diameter. Patten (1935)

M.

kathae D. (Fig. 247,

COCCIDIA
studied
its life

575

cycle and found that during microgametogenesis and

sporogony, 6 chromosomes occur. She added that meiosis occurs in the zygote which is the only diploid stage as in Aggregata eberihi.

Genus Pseudoklossia Leger and Duboscq. Anisogamy and sporogony in the kidney of marine mussels; oocyst or zygote produces numerous spores; spore with 2 sporozoites; no residual body; schizogony unknown, in another host (Leger and Duboscq, 1915, 1917). P. pectinis L. and D. (Fig. 247, c). In kidney of Pecten maximus in France; association of 2 sporozoites which are 3.5/z in diameter.

Spores of Merocystis kathae, X1000 (Foulon); c, Pseudoof a spore, X1470 (Leger and Duboscq); d-k, Eimeria stiedae (d, a trophozoite; e, host cell with three trophozoites; f, g, schizogony; h, macrogametocyte, X1270 (Hartmann) i-k, oocysts, X830 (Wasilewski)); 1, m, E. perjorans, X750 (Perard); n, E. faurei,
Fig. 247.
a, b,

klossia pectinis,

two sporozoites

X800 (Wenyon).

Genus Caryotropha

Siedlecki.

Both schizogony and sporogony

take place in a host. One species. C. mesnili S. In coelom (in floating bundles of spermatogonia) of the polychaete, Polymnia nebulosa; schizogony in bundle of spermatogonia, in which cytomeres with 10-16 nuclei and then mero-

formed; schizogony repeated; gametocytes undergo dealso in the same host cells; microgametes become set free in coelom, where union with macrogametes takes place; each oocyst forms about 16 spores; spore with usually 12 sporozoites; cysts are extruded with the reproductive cells of the host worm.
zoites are

velopment

576

PROTOZOOLOGY

Genus Myriospora Lermantoff. Anisogamy and sporogony in marine snails; schizogony unknown; oocyst forms numerous spores each with 2 sporozoites. One species. M. trophoniae L. In the polychaete, Trophonia plumosa; macrogametes, vermiform, up to 800ju long, later ovoid; microgametocyte forms first about 100 cytomeres, each with some 20 nuclei; microgametes comma-shaped; anisogamy; oocyst with several hundred spores, each with about 24 sporozoites. Genus Hyaloklossia Labbe. Schizogony unknown; sporogony in the kidney of marine mussels; oocyst in the organ-cavity; spherical spores of 2 kinds: smaller one with 2 spirally coiled sporozoites and the other with 4-6 sporozoites. One species.
8/x

H. pelseneeri Leger. Spherical oocysts 75-SOfj. in diameter; spores and 11 12^ in diameter; in kidney of Tellina sp. and Donax sp. Genus Angeiocystis Brasil. Schizogony unknown; sporogony in polychaetes; oocyst forms 4 spores; spore oval, with about 30 sporozoites and residual body at a pole. One species. A. audouiniae B. In the cardiac body of Audouinia tentaculata; macrogametes vermiform, up to 65/z long.

Family 3 Dobelliidae Ikeda

Numerous microgametes develop from each microgametocyte;

the union of gametocytes begins early.
schizonts and macroschizonts;

Genus Dobellia Ikeda. Schizonts sexually differentiated: microyoung schizonts binucleate; associaare formed
in

tion of 2 gametocytes begins early as in Adeleidea (p. 590), but

many microgametes
species (Ikeda, 1914).

each microgametocyte. One

D. binucleata

I.

In the gut of Petalostoma minutum; mature oocyst

20-25ju in diameter, with a thin wall, contains

some 100 sporozoites

without any spore membrane around them.

Family 4 Eimeriidae Leger

Macro- and micro-gametocytes develop independently; microgametocyte produces many gametes; an oocyst from a pair of
anisogametes
;

oocyst with variable

number

of spores containing

which condition is used as basis of generic differentiation. Oocysts found in the faeces of hosts are usually immature; time needed for completion of spore formation depends upon the species, temperature, moisture, etc. Becker (1934) recommends the following bactericidal solutions in which oocysts develop
sporozoites,
to maturity:

1-many

1%

formaldehyde,

1%

chromic acid of

2-4%

potas-

sium dichromate.

COCCIDIA

577

Genus Eimeria Schneider {Coccidium Leuckart). Zygote or oocyst produces four spores, each with two sporozoites. Numerous species (Levine and Becker, 1933: Boughton and Volk, 1938; Hardcastle,
1943); host specificity (Becker, 1933).

E. schubergi (Schaudinn) (Fig. 243). In the gut of Lithobius forficatus; oocysts spherical, 22-25/* in diameter.

d-k). In the epithelium of the bile-duct

E. stiedae (Lindemann) {Coccidium oviforme Leuckart) (Fig. 247, and liver (with white nodules) of wild and domestic rabbits; schizonts ovoid or spherical, 1518/i in

diameter; merozoites 8-10/* long; oocysts ovoid to ellipsoid,

often yellowish, micropylar end flattened; mature oocysts 28-40/*

to be fatal to

60-70 hours; heavy infection is believed young animals, which may occur in an epidemic form. Transmission and comparison with E. perforans (Uhlhorn, 1926).

by

16-25/*; sporulation in

E. perforans (Leuckart) (Fig. 247,

sporulation in 48 hours at

I,

m). In the small intestine of

by 14-20/*; 33C; the thermal death point of immature oocysts 51C. (Becker and Crouch, 1931); pathogenic. Other species (Perard, 1925; Becker, 1934). Lund (1950) found 17 per cent
rabbits; oocysts with equally rounded ends, 24-30/*
of coccidian infection

among 1200

faecal specimens collected

from
ellip-

23 commercial rabbitries in southern California.

E.

zilrnii (Rivolta).

In the gut of cattle; oocystss pherical to

soidal, 12-28/*

by

10-20/*; sporulation in

48-72 hours; said to cause

diarrhoea.

E. bovis (Ziiblin) {E. smithi Yakimoff and Galouzo). In the gut of

cattle; oocysts 23-34/*
in

by

17-23/*; sporulation in three to five

days

shallow dishes, and two weeks in deep dishes (Becker). Developet

ment (Hammond

ah, 1946).
a).

E. ellipsoidalis Becker and Frye (Fig. 248,

In the faeces of

calf;

oocysts ellipsoidal, 20-26/* by 13-17/*; sporulation in 18 days (Becker

and Frye,

1929).

E. cylindrica Wilson. In the faeces of cattle; oocysts cylindrical, 19-27/x by 12 15m; sporulation in two to 10 days. E. wyomingensis Huizinga and Winger. In the faeces of cattle;
oocysts pyriform, 37-45/*

by 26-31/*; spores

19/*

by 3/* (Huizinga and

Winger, 1942).
E. faurei Moussu and Marotel (Fig. 247, ri). In the gut of sheep and goat; oocysts ovoid, 20-40 /* by 17-26/*; sporulation in 24-48
hours.

E. arloingi Marotel. In the gut of sheep and goat; oocysts with a

cap, ovoid, 25-35/*

by

18-25/*; sporulation in three days.

E. intricata Spiegel. In the gut of sheep and goat; oocysts with

578

PROTOZOOLOGY

and Frye);

Fig. 248. Oocysts of Eimeria. a, Eimeria ellipsoidalis, XI 500 (Becker b, E. debliecki, X1070 ("Wenyon); c, E. canis, X650 (Wenyon); d, E. falciformis, X730 ( Wenyon); e, E. separata; f, E. miyairii, X2000 ("Becker, Hall and Hager); g, E. mephitidis, X1000 ("Andrews); h, E. cynomysis, X1000 ("Andrews); i. E. citelli, XI 360 ("Kartchner and Becker), X1630 (Fish); k, E. tenella, X600 (Tyzzer); 1, E. mitis, j, E. monads, X430 (Tyzzer); m, E. acervulina, X430 (Tyzzer); n, E. maxima, X470
nil); q,

(Tyzzer;) o, E. ranarum, X670; p, E. prevoti, X670 CLaveran and MesE. ranae, X670 (Dobell); r, E. sardinae, X600, s, E. clupearum. X600 (Thomson and Robertson); t, E. brevoortiana (Hardcastle).

COCCIDIA

579

thick wall, with or without cap, ellipsoidal, 42-60/* by 30-36/*; sporulation in

about 9 days. Species in North American sheep (ChristenRocky Mountain Bighorn sheep (Honess, 1942). E. debliecki Douwes (Fig. 248, &). In the gut of pigs; 30-82 per cent infection in California (Henry); oocysts 12-29/* by 12-20/*; sporulation in seven to nine days. Development (Noller and Frenz, 1922). E. scabra Henry. In the caecal contents of pigs; oocysts, brown, elsen, 1938), in
lipsoidal, 22-36/*

by

16-26/*.

Henry (1931) recognized 2 other

species

in California swine.

E. caviae Sheather. In the gut of guinea pigs; oocysts subspherical

to ellipsoid, 13-26/*

by

13-22/* (Sheather, 1924).

Morphology and
ellip-

development (Lapage, 1940).

E. cants
hours.

Wenyon
by

(Fig. 248, c). In the

gut of dogs; oocysts,

soidal, 18-45/t

11-28/*; spores 9.5/t

by

2.5/*;

sporulation in 24

E.felina Nieschulz. In the gut of cat; oocysts 21-26/* by 13-17/*.

E. falciformis (Eimer) (Fig. 248, d). In the gut of mice; oocysts
spherical to ovoid, 16-21/*

by 11-17/*; sporulation in 3 days. E. nieschulzi Dieben. In the small intestine of rats; oocysts 16by
13-21/*; sporulation in
of feeding stuffs (Becker, 1941

26.4/*

potency
1943).

65-72 hours. Growth-promoting Becker, Manresa and Smith,

;

E. separata Becker and Hall (Fig. 248,

of rats; oocysts 13-19.5/*

e).

In the caecum and colon

by

11-17/*; sporulation in 27-36 hours.

E. miyairii Ohira (Fig. 248, /). In the small intestine of rats; oocysts 16.5-29/* by 16-26/*; sporulation in 96-120 hours. Unsporulated oocysts perish in 15 seconds at 53C.

and

in

24 hours at 41C.

sporulated oocysts are killed in two minutes at 52C. (Reinhardt

and Becker, 1933). Structure of oocyst wall (Henry, 1932); Eimeria in rodents (Fish, 1930; Henry, 1932a; Roudabush, 1937a).
E. mephitidis Andrews (Fig. 248, g). In the faeces of the common skunk; oocysts oval to spherical, 17-25/* by 16-22/*; wall 1/* thick; a circular micropyle; spores with a rostrum, 10-12/* by 7-9/*; extended sporozoites 10-14/* by 4-5/*; other stages unknown (Andrews, 1928).

E. cynomysis A. (Fig. 248,

cysts oval, 33-37/*

h).

In the faeces of the prairie dog; oo-

by

28-32/*; a double fibrous wall, 1.5-2.5/* thick;

the inner wall slightly orange-yellow; micropyle 5-6 /* in diameter; spores, broad pyriform, 13-17/* b}^ 8-12/*.
E.
citelli

of the striped

Kartchner and Becker (Fig. 248, i). In the caecal contents ground squirrel, Citellus tridecemlineatus; subspherical

to ellipsoidal oocysts 15-23/*

by

14-19/*.

580

PROTOZOOLOGY

Fig. 249. Diagram illustrating the development of Eimeria tenella in the caecal glands of chick (Tyzzer). The numbers below indicate the days of infection, ma, macrogamete; me, merozoite (me 1 me 2 me 3 generation 1, 2, 3 merozoites respectively); mi, microgametocyte; oo, oocyst; ret. oo and ret. sch, oocysts and schizonts which failed to escape; sch 1 sch 2 schizonts of generation 1 and 2; tr, young growing trophozoites. (Continue
, , ,

to

upper

left of Fig. 250.)

E. monads Fish (Fig. 248, j). In the intestine of the woodchuck, Marmota monax; spherical to subspherical oocysts 20/a by 18ju (Fish,
1930), 14-20/i in diameter (Crouch

and Becker, 1931) wall compara;

tively thick; sporulation completed in 60-64 hours in 2 per cent po-

tassium bichromate at room temperature. Crouch and Becker found two other species: E. perforoides and E. os, in the woodchuck in
Iowa. Eimeria in lemming (Levine, 1952). E. tenella (Railliet and Lucet) (Figs. 248, k; 249; 250). In the caeca, colon and lower small intestine of chicken; a cause of acute coccidiosis

characterized

by haemorrhage (Tyzzer)

in the caecal contents of

California quail (Henry); oocysts 19.5-26/x

by 16.5-23^; sporula-

tion in 48 hours. Tyzzer's observation on experimental infection in

COCCIDIA

r.si

Fig. 250. Continuation of the diagram shown in Fig. 249 (Tyzzer). the right end of the upper figure continue to the left of the lower figure; for explanation see Figure 249.

From

chicken

is

as follows (Figs. 249

and 250)

When

a large

number

of

582

PROTOZOOLOGY
spores, in as early as 20 hours

oocysts are fed to chickens, the sporozoites emerge from the oocysts

and

and are found on the surface

of the

of

the caecal mucosa.

Toward the end

second day, growing

trophozoites are found in the gland epithelial

cells; they undergo schizogony (Fig. 249, sch 1 ) by the middle of the third day. A single first generation schizont is estimated to produce about 900 pyriform merozoites which measure 2-4 /x by 1-1. 5/x and occur in the gland

lumen (we

).

As

these merozoites invade the epithelial cells of the

cells

fundi of the glands and become trophozoites, the infected host

increase in size,

become rounded and no longer form a continuous layer (tr). These trophozoites (Fig. 250, sch) grow to much greater dimensions (up to as much as 45m in diameter) than those of the 2 first generation and multiply into merozoites (me ) by the fifth day. These merozoites are much larger and more elongated than those of the first generation and measure 16m by 2/x. The haemorrhage in the affected mucosa which begins usually with the growth of the second generation trophozoites, increases in volume so that by the fifth day after infection, a great portion of the mucosa sloughs off, which coincides with the liberation of the merozoites. The merozoites formed in the host cells located in the deeper part of the mucosa are unable to become free and appear to grow into multinucleate forms (ret sch). When the liberated merozoites enter epithelial cells, most of them develop into macrogametocytes (ma) and microgametocytes (mi), while comparatively small numbers become trophozoites and form by budding a few, large third generation merozoites (me 3 ). Mature oocysts (oo) are found on seven to eight days after infection.
Eimeria species in chicken (Tyzzer, 1929, 1932; Henry, 1931a); economic importance (Foster, 1949; Brackett and Bliznick, 1950) pathological changes (Tyzzer, 1929, 1932; Mayhew, 1937); statistical study of infections (Fish, 1931); mortality of hosts (Mayhew, 1933); killing oocysts (Fish, 1931a); control measures (Andrews and Tsuchiya, 1931; Andrews, 1933); comparative oocyst production (Brackett
;

and

Bliznick, 1950); in wild fowls (Haase, 1939).

I).

E. mitis Tyzzer (Fig. 248,

chicken; oocysts subspherical; 16.2m hours (Tyzzer, 1929).

In the anterior small intestine of by 15.5m; sporulation in 48

E. acervulina T. (Fig. 248, m). In the anterior small intestine of

chicken, and in California quail (Henry); oocysts oval, 17. 7-20. 2m

by

13. 7-16. 3m; sporulation in 20 hours; associated with serious chronic coccidiosis (Tyzzer, 1929). Effect on host (Moynihan, 1950).

E.

maxima

T. (Fig. 248, n). In the small intestine of chicken; oo-

cysts oval, 21.5-42.5m

by

16.5-29.8/x (Tyzzer, 1929).

COCCIDIA

583

E. necatrix Johnson. In the small intestine (schizonts) and caeca (oocysts) of chicken; a cause of chronic coccidiosis; oocysts obovate,

13-23 n by 11-18/*; sporulation in 48 hours (Tyzzer, 1932). E. praecox J. In the upper third of the small intestine of chicken; oocysts ovoid, 20-25/* by 15.5-20/*; sporulation in 48 hours. E. meleagridis Tyzzer. In the caeca of turkey; apparently nonpathogenic; oocysts, ellipsoidal, 19-30/x by 14. 5-23 /* (Tyzzer, 1927,
1932). Coccidiosis in turkey (Hawkins, 1952).

what

E. meleagrimitis T. In the lower small intestine of turkey; somesimilar to E. mitis; oocysts, 16.5-20.5/* by 13.2-17.2/* (Tyzzer,
E. adenocides

1929).

of turkeys; oocysts

Moore and Brown. In the ileum, caeca and rectum about 25.6/* by 16.5/*; highly pathogenic to young

turkeys (Moore and Brown, 1950).

E. truncata (Railliet and Lucet). In the kidney of geese; oocysts
truncate at one pole, ovoid, 14-23/* by 13-18/*; some observers find
this coccidian fatal to

young

geese.

E. anseris Kotlan. In the intestine of geese; oocysts spherical or

pyriform, 11-16/* in diameter. Coccidia in
1952a).

Canada goose

(Levine,

E. labbeana Pinto. In the gut of domestic pigeon; oocysts some-

times light brown, 15-26/*

by

14-24/*.

E. dispersa Tyzzer. In the small intestine of bob-white quail and

pheasant; oocysts ovate, 18.8-22.8/* (quail), smaller in pheasant,

without polar inclusion; sporulation in about 24 hours. E. amydae Roudabush. In the intestine of Amyda spinifera; oocysts oval with a thin wall, 17-24/* by 12-17/*; elliptical spores about 11-16/x long (Roudabush, 1937). E. chrysemydis Deeds and Jahn. In the intestine of Chrysemys marginata; oval oocysts 21-27/* by 13-18/*; fusiform spores 12-14/* by 5-8/* (Deeds and Jahn, 1939). Other reptilian species (Roudabush, 1937)
o). In the gut epithelium (nuclei) of about 17/* by 12/*. E. prevoti (Laveran and Mesnil) (Fig. 248, p). In the gut epithelium of frogs; oocysts about 17/* by 12/*. E. ranae Dobell (Fig. 248, q). In the gut of frogs; oocysts 22/* by

E. ranarum (Labbe) (Fig. 248,

frogs; oocysts

18/x.

Species of Eimeria are often parasitic in fishes used for human consumption, and thus may appear in faecal matter. A few examples will be mentioned here. E. sardinae (Thelohan) (E. oxyspora Dobell) (Fig. 248, r). In the

584

PROTOZOOLOGY
oocyst 30-50/u (Thelohan, 1890; Dobell,
s).

testis of sardine; spherical

1919).

E. clupearum (Thelohan) (E. wenyoni Dobell) (Fig. 248,

liver of herring, mackerel,

In the

and sprat; spherical oocysts 18-33^ in diameter (TMohan, 1894; Dobell, 1919). Taxonomy (Thomson and
Robertson, 1926).

Gadus virens, G. morrhua, and sporogony; germination of spores takes place in the bladder of the same host individual, bringing about a very heavy infection; oocysts 26-28 m; pathogenic (Fiebiger,
E. gadi Fiebiger. In the swim-bladder of
aeglefinus; schizogony

and G.

1913).

E. brevoortiana Hardcastle (Fig. 248, t). Schizogony in the epithelium of the pyloric caeca and sporogony in the testis of the menhaden, Brevoortiana tyrannus; mature oocysts, spherical, 17.5-30>
in

diameter or ovoid, 21-30/x by 15-27. 5m (Hardcastle, 1944). Genus Jarrina Leger and Hesse. Oocysts ovoid, one end rounded and the other drawn out into a short neck; 4 spores, each with 2 sporozoites (Leger and Hesse, 1922). J. paludosa L. and H. (Fig. 251, a, b). In the gut of Fulica atra and Gallinula chloropus; oocysts 15/x by 11/x; sporulation in 15 days.

Fig. 251. Oocysts of Coccidia.

;

a,

b,

Jarrina paludosa,

X800 (Leger

and Hesse) c, d, oocyst and spore of Wenyonella africana, X 1330 (Hoare), e, f, a young and a mature oocyst of Isospora hominis, XI 400 (Dobell); g, /. bigemina; h, /. rivolta, X930 (Wenyon).

Genus Wenyonella Hoare. Oocysts with 4 spores, each with 4 Three species. W. africana H. (Fig. 251, c, d). In the small intestine of Boaedon lineatus ("brown snake") in Uganda; oocysts ovoid or subspherical, 18.5 19.2/u by 16-17. 6/x; spores ovoid, 9.6^ by 8yu; sporulation in
sporozoites.

5-6 days.

W.

gallinae

Ray. In the epithelium

of the lower intestine of chick-

COCCIDIA
en; oval oocysts, 29.5-33.5/u

585
18.8/*

by 20-23^; spores

by 8m; sporo-

zoites club-shaped; sporulation in four to six

days at 28C. (Ray,

1945).

taining four sporozoites.

Genus Isospora Schneider. Oocyst produces two spores, each conAvian Isospora (Boughton, Boughton and
/.

Volk, 1938).

hominis (Rivolta)
is

(/. belli

Wenyon)

(Fig. 251,

e,

/).

This

is

the
life

sole coccidian parasite of

man known up

to the present time. Its

unknown, but most probably the schizogony, gametogenesis and sexual fusion occur in the intestinal epithelium. Oocysts have
cycle

only been seen in the stools of infected persons.

The oocyst is asymmetrically fusiform; 20-33^ by 10-16/*; wall is made up of two membranes which are highly resistant to chemicals; when voided in faeces, the contents either fill up the oocyst or appear
as a spherical mass,

composed

of refractile granules of various sizes;

when the faecal specimen kept in a covered container at the room temperature, the protoplasmic mass divides into 2 spherical sporoblasts in about 24 hours
nucleus appears as a clear circular area;
is

each sporoblast develops in another 24 hours into a spore (10-16^ by 7-10m) containing 4 sporozoites. Further changes take place when
the oocyst finds
its

way

into the

human

intestine in

contaminated

food or water.
/.

hominis has been observed

in

widely separated regions, but ap-

As to its effect on the human known. Connal (1922) described the course of an accidental oral infection by viable mature oocysts, as follows: The incubation period was about six days, the onset sudden, and the duration over a month. The cure was spontaneous. The symptoms were diarrhoea, abdominal discomfort, flatulence, lassitude, and loss of weight. During the first three weeks of the illness no oocysts were found, but then oocysts appeared in the stools for nine days. On the 10th day they were not seen, but reappeared on the 11th and 12th days, after which they were not found again. The acute signs of illness abated within one week of the finding of the oocysts. The faeces
pears not to be of

common

occurrence.

host, very little

is

contained a large amount of undigested material, particularly fat which gave it a thick oily consistency, showing signs of slow gaseous
formation.

Japan.

Matsubayashi and Xozawa (1948) found six cases of infection in A volunteer ingested some 3000 oocysts. Eight days later diarrhoea developed, followed by a rise of temperature above 39C, which lasted for 10 days. On the following day, the diarrhoea subsided, but later returned and was especially pronounced on the 17th

586

PROTOZOOLOGY

day, after which it disappeared completely. Oocysts were discharged regularly since the 9th day for 32 days. About a month after the

some 2500 but no infection resulted, which the two authors attributed to the immunity produced during the first infection. Another volunteer showed a similar course of infection. The symptoms disappeared without medication after the termination of oocyst discharge. Thus, the coccidiosis of man appears to be a self-limited one. Attempts to infect common laboratory animals with this coccidian have so far failed (Foner, 1939; Herrlich and Liebmann, 1944; Rita and Vida, 1949). History (Dobell, 1919); human species (Dobell, 1926); incidence (Magath, 1935; Barksdale and Routh, 1948). I. bigemina (Stiles) (Fig. 251, g). In the gut of cat and dog; oocysts
cessation of oocyst-production, the person ingested again
cysts,

10-14/*

by

7-9/x.

I. rivolta (Grassi) (Fig.

251, h). In the gut of cat

and dogs; oocysts

20-25m by
I. felis

15-20/*.

Wenyon

(Fig. 252, a). In cat

and dog; oocysts 39-48/* by

26-37/*.
I.

suis Biester.

In swine faeces; oocysts subspherical, about

22.5/*

by

19.4/*;

sporulation in 4 days.

I. lacazii

Labbe. In the small intestine of passerine birds (spar18-29.2/*; spores, 16.5-18.5/*

rows, blackbirds, finches, etc); oocysts subspherical or ovoidal,

18.5-30/x

by

by

10.3-12.4/*; heavily in-

fected sparrows

show

definite

symptoms

of infection; sporulation in

24 hours (Henry, 1932b). Sparrows and other common small birds have been known to be free from Eimeria infection, while the barnyard fowls are seldom infected by Isospora (Boughton, 1929). Significance of size variation in oocysts (Boughton, 1930; Henry, 1932b)

development (Chakravarty and Kar, 1944). I. buteonis Henry. In the duodenal contents of several species of hawks: Buteo borealis, B. swainsoni, Accipiter cooperii, and Asio flammeus; oocysts irregular in form with a thin wall, 16-19.2/* by
12.8-16/*: spores 9.6-13/*
I.

by

8-10.4/* (Henry, 1932b).

b).

Ueberkiihni (Labbe) (Fig. 252,

frogs.

Oocyst about

40/* long; in the

kidney of

Development

(Noller, 1923).

Genus Cyclospora Schneider. Development similar to that of Eimeria; oocyst with 2 spores, each with 2 sporozoites and covered

by a bi-valve

shell.

C. caryolytica

Schaudinn

(Fig. 252, c). In the gut of the

mole;

sporozoites enter and develop in the nuclei of gut epithelial cells;

oocyst oval, about

15/* by 11.5/*. Development (Tanabe, 1938). Genus Dorisiella Ray. Zygote develops (without becoming oocyst)

COCCIDIA

587

Fig. 252.

a,

Isospora

felis,
c,

X930 (Wenyon); b

/. lieberkuhni,

X660

Cyclospora caryolytica, X1330 (Schaudinn); d, Dorisiella scolelepidis, oocyst with two spores, X1400 (Ray); e, f, Caryospora simplex, XSOO (L6ger); g-i, Cryptosporidium muris (g, h, oocysts; i, emergence of four sporozoites), X1030 (Tyzzer); j, Pfeifferinella ellipsoides, X1330 (Wasielewski) k, P. impudica, X800 (Lger and Hollande) 1, Lankesterella minima, a mature cyst in endothelial cell, XlOOO (Noller); m, Barrouxia ornata, X1330 (Schneider); n. Echinospora
; ;

(Laveran and Mesnil);

labbei,

XlOOO

(Leger).

macrogametocytes migratory. In the gut of the polychaete, Scolelepis fuliginosa; zygote contents divide into 2 oval spores, 1216m by 6-10/x; spore with 8 sporozoites (Ray, 1930). Genus Caryospora Leger. Oocyst develops into a single spore
into 2 spores, each with 8 sporozoites;

D. scolelepidis R.

(Fig. 252, d).

with 8 sporozoites and a residual mass; membrane thick and yellow.

One

species.

C. simplex L. (Fig. 252, e,f). In the gut-epithelium of Vipera aspis;

oocyst thick-walled, 10-1 5^ in diameter.

Genus Cryptosporidium Tyzzer. Lumen-dwelling minute organisms; oocyst with 4 sporozoites.

C. muris T. (Fig. 252, g, i). In the peptic glands of the mouse; both schizogony and sporogony in the mucoid material on surface of the epithelium: oocysts 7/x by 5ju; 4 sporozoites, 12-14/* long (Tyzzer, 1910).

588
C.

PROTOZOOLOGY
parvum T. In the glands
4.5/* in

of small intestine of the

mouse; oocysts

diameter (Tyzzer, 1912). Genus Pfeifferinella Wasielewski. Macrogamete with a "reception tubule" by which microgamete enters; oocyst produces directly
with 4 sporozoites,
8 sporozoites.

P. ellipsoidcs

W.

(Fig. 252, j). In the liver of Planorbis corneus;

oocysts oval, 13-15/* long.

P. impudica Leger and Hollande (Fig. 252, k). In the liver of Limax marginatus; oocysts ovoid, 20/* by 10/*. Genus Lankesterella Labbe. Oocyst produces 32 or more sporozoites directly without spore-formation; in endothelial cells of cold-

blooded vertebrates; mature sporozoites enter erythrocytes in which they are transmitted to a new host individual by bloodsucking invertebrates. L.

minima (Chaussat)

(Fig.

252,
;

I).

In frogs; transmitted by

the leech (Placobdella marginata)

introduction of sporozoites

frog acquires infection through

by a

leech; sporozoites

make

their

way

into the blood capillaries of various organs; there they enter endo-

schizogony produces numerous merozoites which bring about infection of many host cells; finally macro- and micro-gametocytes are formed anisogamy produces zygotes which transform into oocysts, in which a number of sporozoites develop; these sporozoites are set free upon disintegration of cyst wall in the blood plasma and enter erythrocytes (Noller) oocyst oval, about 33/* by 23/*. Genus Schellackia Reichenow (Tyzzeria Allen). Oocyst spherical with 8 sporozoites, without spore membrane; in the intestine of birds and lizards. S. bolivari R. In the mid-gut of the lizards, Acanthodactylus vulgaris and Psammodromus hispanicus; development somewhat similar to that of Eimeria schubergi (Fig. 243) oocysts spherical, 15-19/* in diameter, with 8 sporozoites (Reichenow, 1919).
thelial cells;
;
;

S. perniciosa (Allen). In the small intestine of

Anas domesticus;

oocysts 10-13.3/*

by

9-10.8/*; highly pathogenic.

Genus Barrouxia Schneider. Oocyst with numerous spores, each with a single sporozoite; spore membrane uni- or bi-valve, with or without caudal prolongation. Development (Schellack and Reichenow, 1913).
B. ornata S. (Fig. 252, m). In gut of
cal,

Nepa

cinerea; oocysts spheri-

34-37/* in diameter, with

many spores; spore with one sporozoite

spores, each with a

and bivalve shell, 17-20/* by 7-10/*. Genus Echinospora Leger. Oocyst with 4-8
sporozoite; endospore with

many

small spinous projections.

COCCIDIA

589

E. labbei L. (Fig. 252, n). In the gut of Lithobivs mvtabilis; oocyst spherical, 30-40ai in diameter; spores, 11m by 9.4/u, with bi-valve
shell; sporulation

completed in about 20 days.

Fig. 253. The life-cycle of Adelea ovata, XtiOO (Schellack and Keichenow). a, schizont entering the gut epithelium of the host centipede; b-d, schizogony; e, larger form of merozoite; f, microgametocyte (left) and macrogametocyte (right) g, association of gametocytes; h, i, fertilization; zygote; k, nuclear division in zygote; 1, mature oocyst with many j,
;

spores.

590

PROTOZOOLOGY
Suborder 2 Adeleidea Leger

The Adeleidea

are on the whole similar to Eimeridea in their

habitat and development, but the micro- and macro-gametocytes

become attached to each other in pairs during the course of development into gametes (Fig. 253), and each microgametocyte produces a few microgametes. The zygote becomes oocyst which produces numerous sporoblasts, each of which develops into a spore with 2 or
4 sporozoites.
In epithelium of gut and
In
cells of circulatory
its

appended glands
of vertebrates

of chiefly invertebrates.

Family
system

Adeleidae
(p.

Family 2 Haemogregarinidae

592)

Family

Adeleidae Leger

Genus Adelea Schneider. Zygote develops into a thinly walled oocyst with numerous flattened spores, each with 2 sporozoites; in
arthropods.

A. ovata S. (Fig. 253). In the gut of Lithobius forficatus; merozoites 17-22^ long; oocysts elongate oval, 40-50/z by 30-40m; 17-33 or

more

by 4/z (Hesse, 1910a). and Reichenow, 1913, 1915). Genus Adelina Hesse. Oocyst thick-walled; spores spherical, comparatively small in number; in the gut or coelom of arthropods and
spores; spores circular, flattened, 20m
Life cycle (Schellack

oligochaetes (Hesse, 1910, 1910a).

cingulata
1913).

A. dimidiata (Schneider) (Fig. 254, a). In the gut of Scolopendra and other myriapods; oocysts with 3-17 spores (Schellack,
b).

A. octospora H. (Fig. 254,

Spherical oocyst contains spores; in

the coelom of Slavina appendiculata (Hesse, 1910a).

A. deronis Hauschka and Pennypacker. In peritoneum of Dero

limosa; oocyst contains 12 (10-14) spores; meiosis at the
first

zygotic
is

nuclear division; haploid chromosome

number

10; the life cycle

days at room temperature (Hauschka, 1943). Genus Klossia Schneider. Oocyst with numerous spherical spores, each with 3-10 sporozoites. Several species. Life cycle (Xabih, 1938). K. helicina S. In the kidneys of various land-snails, belonging to genera Helix, Succinea, and Vitrina; oocyst with a double envelope 120-180/z in diameter; spores 12/x in diameter, with 5-6 sporozoites (Debaisieux, 1911). Cytology and development (Naville, 1927). Genus Orcheobius Schuberg and Kunze. Macrogametes vermiform; oocyst with 25-30 spores, each with 4 (or 6) sporozoites.
completed
in 18

COCCIDIA

591

b, A. octoOrcheobias herpobdellae, X550 (Kunze); d, e, Klossiella muris (d, renal cell of host with 14 sporoblasts; e, spore), X280 (Smith and Johnson); f, Legerella hydropori, oocyst, XlOOO (Vincent); g, h, Haemogregarina of frog, X1400 (Kudo); i-m, H. simondi, in the blood of the sole, Solea vulgaris, X1300 (Laveran and Mesnil);

Fig. 254.

a,

Adelina dimidiata, a spore, XlOOO (Schellack);

c,

spora, oocyst,

XlOOO (Hesse);

n,

Hepatozoon muris, spore, X420 (Miller); (Reichenow).

0. herpobdellae S.

o,

Karyolysus

lacertae,

X700

and K.

(Fig. 254, c).

In the

testis of Herpobdella

atomaria; mature macrogametes 180^

by

30//;

microgametes 50m

by 12/x; schizogony in April and May; sporogony in June and July. Genus Klossiella Smith and Johnson. Microgametocyte produces 2 microgametes; oocyst with many spores, each with numerous sporozoites; in the kidney of mammals (Smith and Johnson, 1902). K. muris S. and J. (Fig. 254, d, e). Oocyst with 12-14 spherical spores; about 30-34 sporozoites in a spore, 16/x by 13/j; spores discharged in the host's urine; in the epithelium of the tubules and
glomeruli in the kidney of the mouse,

Mus

musculus.

Oocyst with 8-20 spores; spore with about 30 sporozoites; in the kidney of guinea pig. Genus Legerella Mesnil. Oocyst contains numerous sporozoites; spores entirely lacking; in arthropods (Mesnil, 1900). L. hydropori Vincent (Fig. 254,/). In the epithelium of Malpighian

K. cobayae

Seidelin.

592

PROTOZOOLOGY

tubules of Hydroporus palustris; oocysts ovoid, 20-25// long, with

16 sporozoites which measure 17m

by 3m (Vincent, 1927). Genus Chagasella Machado. Oocyst with 3 spores, each with 4

or 6 (or more) sporozoites; in hemipterous insects.

C. hartmanni (Chagas). In the gut of Dysdercus ruficollis; oocysts with 3 spores about 45m in diameter; spore with 4 sporozoites, about

35m by 15m (Machado, 1911). Genus Ithania Ludwig. Microgametocyte produces four microgametes; oocyst with one to four spores, each with nine to 33 sporozoites.

One

species (Ludwig, 1947).

L. In the epithelial cells of the gastric caeca and midgut of the larvae of the crane-fly, Tipula abdominalis; oocysts 34I. weririchi

63m by 22-50m-

Family 2 Haemogregarinidae Leger

With 2

hosts: vertebrates (circulatory system)

and invertebrates
in

(digestive system)

blood

Genus Haemogregarina Danilewsky. Schizogony takes place cells of vertebrates; when gametocytes are taken into gut

of

leech or other blood-sucking invertebrates, sexual reproduction takes

place; microgametocyte develops 2 or 4 microgametes; sporozoites formed without production of spores. H. stepanowi D. (Fig. 255). Schizogony in Emys orbicularis and

sexual reproduction in Placobdella catenigera; sporozoites introduced

into blood of the chelonian host
in
;

by leech (a), and enter erythrocytes which they grow (d-g) schizogony in bone-marrow, each schizont producing 12-24 merozoites (h); schizogony repeated (i); some merozoites produce only 6 merozoites (j, k) which become gametocytes (l-o); gametogony occurs in leech; 4 microgametes formed from each microgametocyte and become associated with macrogametocytes in gut of leech (p-r) zygote (s) divides three times, and
;

develops into 8 sporozoites (t-w).

Haemogregarines are found commonly

1911), reptiles, amphibians (Fig. 254,

in various birds (Aragao,

g, h)

(Roudabush and Coat-

ney, 1937) and fishes (Fig. 254, i-m).

Genus Hepatozoon Miller. Schizogony in the cells of liver, spleen, and other organs of vertebrates; merozoites enter erythrocytes or leucocytes and develop into gametocytes; in blood-sucking arthropods (ticks, mites), micro- and macro-gametes develop and unite in pairs; zygotes become oocysts which increase in size and produce sporoblasts, spores, and sporozoites. H. muris (Balfour) (Fig. 254, n). In various species of rat; several

COCCIDIA

503

Fig. 255. The life-cycle of Haemogregarina stepanowi, X1200 (Reichenow), a, sporozoite; b-i, schizogony; j-k, gametocyte-formation, 1, m, microgametocytes; n, o, macrogametocytes; p, q, association of gametocytes; r, fertilization; s-w, division of the zygote nucleus to form eight
sporozoites.

594
specific

PROTOZOOLOGY
of difference in host,
so indistinct^ defined

names were proposed on the basis locality, and effect on the host, but they are
liver of rat;

that specific separation appears to be impossible. Schizogony in the

young gametocytes invade mononuclear leucocytes and appear as haemogregarines; when blood is taken in by the mite, Laelaps echidninus, union of 2 gametes produces vermicular body which penetrates gut-epithelium and reaches peri-intestinal tissues and grows; becoming surrounded by a cyst-membrane, cyst content breaks up into a number of sporoblasts and then into spores, each of which contains a number of sporozoites; when a rat devours infected
it becomes infected. Genus Karyolysus Labbe. Sporoblasts formed in the oocysts in gutepithelium of a mite, vermiform sporokinetes, enter host ova and become mature; when young mites hatch, spores in gut-epithelium are cast off and discharged in faeces; a lizard swallows spores; liberated sporozoites enter endothelial cells in which schizogony takes place; merozoites enter erythrocytes as gametocytes which when taken in by a mite complete development in its gut. K. lacertae (Danilewskj^) (Fig. 254, o) In Lacerta muralis;

mites,

sexual reproduction in Liponyssus saurarum; sporokinetes 40-50ju

long; spores 20-25/x in diameter (Reichenow, 1913, 1921).

References

Allen, Ena A.: (1936) Tyzzeria pernisiona,

262.

etc.

Arch. Protist., 87:

Andrews,

from the skunk and 14:193. control of poultry coccidiosis by the chemical treatment of litter. Am. J. Hyg., 14:466. and Tsuchiya, H.: (1931) The distribution of coccidial oocysts on a poultry farm in Maryland. Poultry Sc. 10:320. Aragao, H. B.: (1911) Beobachtungen ueber Haemogregarinen von Vogeln. Mem. Inst. Oswaldo Cruz, 3:54. Barksdale, W. L. and Routh, C. F.: (1948) Isospora hominis infection among American personnel in southwest Pacific. Am. J. Trop. Med., 28:639. Becker, E. R.: (1933) Cross-infection experiments with Coccidia of rodents and domesticated animals. J. Parasitol., 19:230. (1934) Coccidia and coccidiosis. Ames, Iowa. (1941) Effect of parenteral administration of vitamin B 1} etc. Proc. Soc. Exper. Biol, 46:494. and Crouch, H. B. (1931) Some effects of temperature upon development of the oocysts of Coccidia. Ibid., 28:529. and Frye, W. W. (1929) Eimeria ellipsoidalis n. sp., a new coccidium of cattle. J. Parasit., 15:175. and Hall, Phoebe R.: (1931) Eimeria separata, a, new speJ.:

(1928)

New

species of Coccidia

dog. (1933) The

prairie

J. Parasit.,

COCCIDIA
cies of coccidian

595

from the Norway

rat.

Iowa State College

J.

Sc,

6:131.

and Hager, Anna: (1932) Quantitative, biometric and host-parasite studies on Eimeria miyairii, etc. Ibid., 6:299. Manresa, M. Jr. and Smith, L.: (1943) Nature of Eimeria
,

nieschulzi-growth-promoting potency of feeding stuffs. V. Ibid., 17:257. Belar, K.: (1926) Zur Cytologic von Aggregate/, eberthi. Arch. Protist., 53:312. Boughton, D. C: (1929) A note on coccidiosis in sparrows and poultry. Poultry Sc, 8:184. (1930) The value of measurements in the study of a protozoan parasite Isospora lacazei. Am. J. Hyg., 11:212. (1933) Diurnal gametic periodicity in avian Isospora. Ibid., 18:161. (1937) Notes on avian coccidiosis. Auk, 54:500. Boughton, Ruth B. and Volk, J.: (1938) Avian hosts of the genus Isospora. Ohio J. Sc, 38:149. and Volk, J. J.: (1938) Avian hosts of Eimerian Coccidia. Bird Band., 9:139. Brackett, S. and Bliznick, A.: (1950) The occurrence and economic importance of coccidiosis in chickens. 78 pp. Pearl River, N. Y. (1952) The reproductive potential of 5 species of Coccidia of the chicken, etc. J. Parasitol., 38:133. Chakravarty, M. and Kar, A.: (1944) Studies on Coccidia of Indian birds. I. J. Dep. Sc, Calcutta Univ., 1 :78. (1947) A study of the Coccidia of Indian birds. Proc Roy. Soc Edinburgh, 62:225. Christensen, J. F.: (1938) Species differentiation in the Coccidia from the domestic sheep. J. Parasitol., 24:453. Connal, A.: (1922) Observations on the pathogenicity of Isospora hominis, etc. Tr. Roy. Soc. Trop. Med. Hyg., 16:223. Crouch, H. B. and Becker, E. R.: (1931) Three species of Coccidia from the woodchuck, etc. Iowa State College J. Sc, 5: 127.
,

Debaisieux,

P.: (1911) Recherches sur les coccidies. I. La Cellule, 27:89. Deeds, O. J. and Jahn, T. L.: (1939) Coccidian infections of western painted turtles, etc. Tr. Am. Micr. Soc, 58:249. Dobell, C: (1919) A revision of the Coccidia parasitic in man. Parasitology, 11:147. (1925) The life-history and chromosome cycle of Aggregata eberthi. Ibid., 17:1. Fiebiger, J.: (1913) Studien ueber die Schwimmblasencoccidien der Gadus-Arten (Eimeria gadin. sp.). Arch. Protist., 31:95. Fish, F.: (1930) Coccidia of rodents: etc. J. Parasit., 17:98. (1931) Quantitative and statistical analysis of infections with Eimeria tenella in the chicken. Am. J. Hyg., 14:560. (1931a) The effect of physical and chemical agents on the oocysts of Eimeria tenella. Science, 73:292.

596

PROTOZOOLOGY

Foner, A.: (1939) An attempt to infect animals with Isospora belli. Tr. Roy. Soc. Trop. Med. Hyg., 33:357. Foster, A. O.: (1949) The economic losses due to coccidiosis. Ann. New York Acad. Sc, 52:434. Haase, A.: (1939) Untersuchungen ueber die bei deutschen Wildhuhnern vorkommenden Eimeria-Arten. Arch. Protist., 92:329. Hammond, D. M., et al.: (1946) The endogenous phase of the life
cycle of Eimeria bovis. J. Parasitol., 32:409. check list and host index of the species B.: (1943) of the genus Eimeria. Proc. Helm. Soc, 10:35. (1944) Eimeria brevoortiana, etc. J. Parasitol., 30:60. Hawkins, P. A. (1952) Coccidiosis of the turkey. Tech. Bull. Michigan Agr. Exper. Stat., 226, 87 pp. Henry, Dora P.: (1931) A study of the species of Eimeria occurring in swine. Univ. California Publ. Zool., 36:115. (1931a) Species of Coccidia in chickens and quail in Cali-

Hardcastle, A.

fornia. Ibid., 36:157.

Herrlich, A. and Liebmann, H.: (1943) Zur Kenntnis der menschlichen Coccidien. Ztschr. Hyg. Infektionskr., 125:331. (1944) Die menschliche Coccidiose, etc. Ibid., 126:
22.

Hesse, E.: (1910) Protozoaires nouveaux parasites des animaux d'eau douce. II. Ann. Univ. Grenoble, 23:396. (1910a) Sur le genre Adelea, etc. Arch. zool. exper. gen., 7(N-R):15. Honess, R. F.: (1942) Coccidia infesting the Rocky Mountain Bighorn sheep in Wyoming, etc. Bull. Univ. Wyoming Agr. Exper.
Stat., no. 249.

Huizinga, H. and Winger, R. N.: (1942) Eimeria wyomingensis, a new coccidium from cattle. Tr. Am. Micr. Soc, 61 131. Kartchner, J. A. and Becker, E. R.: (1930) Observations on Eimeria citelli, etc J. Parasitol., 17:90. Lapage, G.: (1940) The study of coccidiosis (Eimeria caviae) in the
:

guinea-pig. Veter.

J.,

96:144, 190, 242, 280.

Leger,

L.: (1911) Caryospora simplex, coccidie monosporee et la classification des coccidies. Arch. Protist., 22:71.

and Duboscq, O.: (1915) Pseudoklossia glomerata n.g., n. sp., coccidie de lamellibranche. Arch. zool. exper. gen., 55 (N-R):7. (1917) Pseudoklossia pectinis n. sp., etc. Ibid., 56
(N-R):88. and Hesse, E.: (1922) Coccidies d'oiseaux palustres le genre Jarrina n.g. C. R. Acad. Sc, 174:74. Levine, N. D. (1952) Eimeria dicrostonicis n. sp., a protozoan parasite of the lemming, etc Tr. Illinois Acad. Sc, 44:205. (1952a) Eimeria magnalabia and Tyzzeria sp. from the Can:

ada goose. Cornell Veter., 42:247. and Becker, E. R.: (1933) A catalog and host-index of the species of the coccidian genus Eimeria. Iowa State College J. Sc, 8:83.

COCCIDIA
Ludwig,

597

F. W.: (1947) Studies on the protozoan fauna of the larvae of the crane-fly, Tipula abdominalis. II. Tr. Am. Micr. Soc, 66: 22. Lund, E. E. (1950) survey of intestinal parasites in domestic rabbits in six counties in southern California. J. Parasitol., 36: 13. Machado, A.: (1911) Sobro novo coccidio do intestino de hemiptero. Brazil Med., no. 39. Mackinnon, Doris L. and Ray, H. N.: (1937) coccidian from the eggs of Thalassemia neptuni. Parasitology, 29:457. Magath, T. B.: (1935) The coccidiaof man. Am. J. Trop. Med., 15: 91. Marshall, E. K.: (1950) Infection with Isospora hominis, etc. J. Parasit., 36:500. Matsubayashi, H. and Nozawa, T.: (1948) Experimental infection
:

um

um

of Isospora

Mayhew,

hominis in man. Am. J. Trop. Med., 28:633. R. L.: (1933) Studies on coccidiosis. V. Poultry Sc, 12:

206. (1937) IX. Tr. Am. Micr. Soc, 56:431. Miller, W. W.: (1908) Hepatozoon perniciosum, etc. U.S.P.H. Serv., Hyg. Lab. Bull., no. 46. Moore, E. N. and Brown, J. A.: (1951) new coccidium pathogenic for turkey, Eimeria adenoeides n. sp. Cornell Veter., 41: 124. Moroff, T.: (1908) Die bei den Cephalopoden volkommenden Aggregata-Arten, etc. Arch. Protist., 11:1. Moynihan, I. W.: (1950) The role of the protozoan parasite, Eimeria acervulina, etc. Canada J. Comp. Med. Vet. Sc, 14:

74.

Nabih, A.: (1938) Studien

Protist., 91:474.

iiber die

Gattung Klossia,

etc.

Arch.

Naville, A.: (1925) Recherches sur le cycle sporogonique des Aggregata. Rev. Suisse Zool., 32:125. (1927) Recherches sur le cycle eVolutif et chromosomique de
Klossia
101.
helicis.

Arch. Protist., 57:427.

eines Nierencoccids. Ibid., 47:

Noller, W.: (1923) Zur Kenntnis

and Frenz, O.: (1922) Zur Kenntnis des Ferkelkokzids und Wirkung. Deutsch. tierarztl. Wechonschr., 30:1. Patten, R. (1935) The life history of Merocystis kathae in the whelk, Buccinum undulatum. Parasitology, 27:399. Perard, C. (1925) Recherches sur les coccidies et les coccidioses du lapin. Ann. Inst. Pasteur, 39:505. Pratt, I.: (1940) The effect of Eimeria tenella upon the blood sugar
seiner
:
:

of the chicken. Tr. Am. Micr. Soc, 59:31. Ray, H. N.: (1930) Studies on some Sporozoa in polychaete worms.

Reichenow,

Parasitology, 22:471. E.: (1913) Karyolysus lacertae, etc. Arb. kais. Gesundh. 45:317. (1919) Der Entwicklungsgang der Haemococcidien Karyolysus, etc Sitz-Ber. Gesell. naturf. Fr. Berlin, p. 440.
II.

598

PROTOZOOLOGY

(1921) Die Haemococcidien der Eidechsen. Arch. Protist. 42:179. Reinhardt, J. F. and Becker, E. R. (1933) Time of exposure and temperature as lethal factors in the death of the oocysts, etc. Iowa State College J. Sci., 7:505. Rita, G. and Vida, B. L. D.: (1949) Coccidiosi umana da Isospora. Riv. Parassit., 10:117. Roudabush, R. L.: (1937) Some coccidia of reptiles found in North America. J. Parasitol., 23:354. (1937a) The endogenous phases of the life cycle of Eimeria nieschulzi, etc. Iowa State College J. Sc, 11:135. (1937b) Two Eimeria from the flying squirrel, etc. J. Parasitol, 23:107. and Coatney, G. R.: (1937) On some blood Protozoa of reptiles and amphibians. Tr. Am. Micr. Soc, 56:291. Schaudinn, F.: (1900) Untersuchungen ueber den Generationswechsel bei Coccidien. Zool. Jahrb. Abt. Morphol, 13:197. Schellack, C. (1913) Coccidien-Untersuchungen. II. Arb. kais. Gesundh., 45:269. and Reichenow, E.: (1913) I. Ibid., 44:30. Schneider, A.: (1885) Tablettes zoologiques. 1. Smith, T. and Johnson, H. P.: (1902) On a coccidium (Klossiella muris g. et sp. nov.) parasitic in the renal epithelium of the mouse. J. Exper. Med., 6:303. Tanabe, M.: (1938) On three species of Coccidia of the mole, Mogera wogura coreana, etc. Keijo J. Med., 9:21.
: :

Thelohan,

P.: (1890) Sur deux coccidies nouvelles, parasites de l'epinoche et de la sardine. C. R. Acad. Sc, 110:1214. (1894) Nouvelles recherches sur les coccidies. Arch. zool. exp., 2:541. Thomson, J. G. and Robertson, A.: (1926) Fish as the source of certain Coccidia recently described as intestinal parasites of man. British Med. J., p. 282. Tyzzer, E. E.: (1910) An extracellular coccidian, Cryptosporidium muris, etc. J. Med. Res., 18:487. (1912) Cryptosporidium parvum, etc. Arch. Protist., 26:394. (1927) Species and strains of Coccidia in poultry. J. Parasit., 13:215. (1929) Coccidiosis in gallinaceous birds. Am. J. Hyg., 10:1. (1932) Coccidiosis in gallinaceous birds. II. Ibid., 15:319. Uhlhorn, E.: (1926) Uebertragungsversuche von Kaninchencoccidien auf Huhnerkucken. Arch. Protist., 55:101. Vincent, Mary: (1927) On Legerella hydropori n. sp., etc. Parasitology, 19:394. Wenyon, C. M.: (1933) Coccidiosis of cats and dogs and the status of the Isospora of man. Ann. Trop. Med. Parasitol., 17:231. (1926) Protozoology. 2. London and Baltimore. Zublin, E.: (1908) Beitrag zur Kenntnis der roten Ruhr der Rinde, etc. Schweiz. Arch. Tierheilk., 50:123.

Chapter 26

Order 3 Haemosporidia Danilewsky

on the whole, the Haemosporidia development THE that they undergo asexual reproduction that the Coccidia
of
is,

similar

to

of

in

f ormation

or schizogony, and also sexual reproduction resulting in sporozoitebut the former takes place in the blood of vertebrates and
;

the latter in the alimentary canal of some blood-sucking invertebrates. Thus one sees that the Haemosporidia remain always within the body of one of the two hosts; hence, the sporozoites do not possess

any protective envelope.

The Haemosporidia are minute intracorpuscular parasites of vertebrates. The malarial parasites of man are typical members of this order. The development of Plasmodium vivax is briefly as follows
(Fig. 256).

zoites into

An infected female anopheline mosquito introduces sporohuman blood when it feeds on it through skin (a). The
They are capable of slight movement when seen under the microscope
of exo-eryth-

sporozoites are fusiform and 6-15ju long.

vibratory and gliding

after

removal from mosquitoes. After about 7-10 days

rocytic development (p. 602), the organisms are found in erythrocytes (c, d) and are called schizonts. At the beginning the schizonts

are small rings. They grow and finally divide into 12-24 or more merozoites (e,f) which are presently set free in the blood plasma (g). This schizogony requires 48 hours. The freed merozoites will, if not ingested by leucocytes, enter and repeat schizogony in the erythrocytes. After repeated and simultaneous schizogony in geometric progression, large

numbers

of infected erythrocytes will be destroyed at

intervals of 48 hours, apparently setting free ever-increasing

of toxic substances into the blood. This
is

amounts

the cause of the regular

occurrence of a characteristic paroxysm on every third day. In the meanwhile, some of the merozoites develop into gametocytes instead of undergoing schizogony (h-k).

When

fully

formed

they are differentiated into macro- and micro-gametocytes, but remain as such while in the human blood. When a female anopheline mosquito takes in the blood containing gametocytes, the microgametocyte develops into 4-8 microgametes (k, I), and the macrogametocyte into a macrogamete (i, m) in its stomach. An ookinete
is formed when a microgamete fuses with a macrogamete The ookinetes are motile. As they come in contact with the stomach epithelium, they enter it and become rounded into oocysts which lie between the base of the epithelium and the outer membrane

(zygote)

(m, n).

of the

stomach

(o).

Within the oocysts, repeated nuclear division

599

600

PROTOZOOLOGY
(p).

produces numerous sporozoites

When

fully mature, the oocyst

haemolymph through which they migrate to the salivary glands (g, r). The sporozoites make their way through the gland epithelium and finally to the duct of hypopharynx. They are ready to infect a human victim when the mosquito pierces with its proboscis the skin for another blood meal. Thus the sexual reproduction occurs in the mosquito (primary host) and the asexual reproduction, in man (secondary host). The Haemosporidia are divided into three families:
ruptures and the sporozoites are set free in the

With pigment granules

Schizogony in peripheral blood of vertebrates Family 1 Plasmodiidae Gametocytes in peripheral blood; schizogony elsewhere Family 2 Haemoproteidae (p. 618) Without pigment granules; minute parasites of erythrocytes
.

Family 3 Babesiidae

(p.

622)

Family

Plasmodiidae Mesnil

Genus Plasmodium Marchiafava and Celli. Schizogony in erythrocytes and also probably in endothelial cells of man, mammals, birds, and reptiles; sexual reproduction in blood-sucking insects; widely
distributed.

Numerous

species.

In

all species,

the infection in a vertebrate host begins under natu-

with the inoculation of the sporozoites by a vector mosquito. The form, size and structure of the sporozoites vary widely within a species so that identification of the species in this stage appears to be impossible (Boyd, 1935). Until some 20 years ago, it had
ral condition

been generally believed that the sporozoites upon entering the blood, penetrate and enter immediately the erythrocyte and begin intracorpuscular development, which process Schaudinn (1902) reported to have seen in life. In this the eminent pioneer protozoologist was in error, since no one has up to the present time been able to confirm his observation. Et. and Edm. Sergent (1922) were the first to find that quinine given in large doses to the canaries on the day the birds were bitten by Culex mosquitoes infected with Plasmodium relictum, did not prevent infection in the birds. During the course of studies on
P. vivax in cases of general paresis, Yorke and MacFie (1924) discovered that if quinine was given before the inoculation of infected blood, no infection resulted, but if the sporozoites were inoculated, quinine did not prevent infection. Similar observations were made on other species of malarial organisms. James (1931) suggested the
possibility that the sporozoites are carried

away from

peripheral to

visceral circulation
thelial system.

and develop

in the cells of the reticuloendo-

HAEMOSPORIDIA

601

In.

man.

In.

female

anopheline

mosquito

life-cycle of Plasmodium vivax (Kudo), a, sporozoite enblood; b, exoerythrocytic stage; c, the initiation of the erythrocytic development; d, a young schizont ("ring form"); e-g, schizogony; h, i, macrogametocytes; j, k, microgametocytes; 1, microgamete-formation in the stomach of a mosquito; m, union of the gametes; n, zygote or ookinete; o, rounding up of an ookinete in the stomach wall; p, oocyst in which sporozoites are developing; q, mature oocyst ruptured and sporozoites are set free in the haemolymph; r, sporozoites entering

Fig. 256.

The

tering

human

the salivary gland

cells.

602

PROTOZOOLOGY

Boyd and Stratman-Thomas (1934) found that the peripheral who had been subjected to the bites of 15 anopheline mosquitoes infected by Plasmodium vivax, did not become infectious to other persons by subinoculation until the 9th day and that
blood of a person
the parasites were not observed before the 11th day in the stained
films of the peripheral blood.

Warren and Coggeshall (1937) observed

that

when suspensions

of the sporozoites of P. cathemerium ob-

tained from infected Culex pipiens, were inoculated into canaries,

the blood was not infectious for 72 hours, but emulsions

the spleen, liver and bone

made from

marrow contained infectious parasites which brought about infection by subinoculations in other birds. These and many similar observations cannot be satisfactorily explained if one follows Schaudinn's view. The fact that P. elongatum
is

capable of undergoing schizogony in the leucocytes and reticulo-

endothelial cells in addition to erythrocytes of host birds had been

observed by Raffaele (1934) and Huff and Bloom (1935). As to the nature of development of Plasmodium during the prepatent period, James and Tate (1938) showed that there occur schizonts and schizogonic stages in the endothelial cells of the spleen,
heart, liver, lung,
(Fig. 257).

and brain of the birds infected by P. gallinaceum They suggested the term exo erythrocytic to this schizogony in contrast to the well known erythrocytic schizogony. Huff and his co-workers made a series of detailed studies of pre-erythrocytic
stages of this avian species. According to Huff

and Coulston

(1944).

the sporozoites that are inoculated into the skin of chickens, are engulfed

by phagocytes

in 0.5-6 hours. In heterophile leucocytes, the

sporozoites are apparently killed, but in the cells of lymphoid-

macrophage system they develop into cryptozoites (Huff, Coulston and Cantrell, 1943) by assuming a spheroid shape and increasing in size for the first 36 hours, during which time there is a rapid repeated division of the nucleus. The schizogony is completed in 36 to 48 hours, each giving rise to 75-150 merozoites. These merozoites
enter

new lymphoid-macrophage and

endothelial cells

and become

metacryptozbites which undergo schizogony similar to that of the

cryptozoite. After three or four generations, the merozoites enter

erythrocytes, and thus the erythrocytic stages appear in five to 10

days. Porter (1942) distinguishes two types of exoerythrocytic de-

velopment in avian Plasmodium; namely, gallinaceum-type just quoted and elongatum-type Exoerythrocytic or E.-E. stages were further discovered in saurian Plasmodium (Thompson and Huff, 1944; Garnham, 1950) and in mammalian malaria organisms (Shortt and Garnham, 1948). In P.

HAEMOSPORIDIA

603

Fig. 257. Exoerythrocytic schizogony in avian Plasmodium, a-f, P. gallinaceum in smears from chicks (James and Tate), a, monocyte from lung, infected by 2 young schizonts; b, monocyte from liver, with a growing trinucleate schizont; c, monocyte from lung, with a large multinucleate schizont; d, large mature schizont containing many mature merozoites, free in lung; e, portion of broken schizont from lung, showing the attached developing merozoites. ( X1660). f, a capillary of brain blocked by 3 large schizonts ( X740). g, h, P. cathemerium in sections of organs of canaries (Porter; X1900). g, capillary in the brain, showing an endothelial cell infected with a uninucleate and a multinucleate schizont; h, a multinucleate schizont and a group of merozoites found in a capillary of heart muscle.

cynomolgi, Shortt and

in the

Garnham
cells of
is

report that the E.-E. stages occur

parenchymatous

the liver of host

monkeys and
earliest

are in-

forms were seen on the fifth day after the inoculation of the sporozoites. They are rounded bodies, about 10m in diameter and contain about 50 chromatin granules of irregular shape. They grow in size to about 35m in diameter, and divide in eight to nine days into some 1000 merozoites, each measuring about 1/z. These merozoites presumably invade the erythrocyte. In P. vivax, the E.-E. stages develop in the parenchymatous cells of the liver also and resemble those of P. cynomolgi. The forms found on the seventh day after sporozoiteinoculation were slightly larger (about 42/z in diameter) than those
clined to think that there

one generation only. The

604

PROTOZOOLOGY

of P. cynomolgi, and when mature, give rise to 800-1000 merozoites. Thus exoerythrocytic stages and development have definitely

been demonstrated for Plasmodium in various host groups, although morphological and developmental details, distinction between them and other little known organisms such as Toxoplasma (p. 625) and interrelationship between them and erythrocytic stages, had to be looked for in future investigations (Fig. 258). General review of E.-E. development (Huff, 1947, 1948; Garnham, 1948).

cnosqui

HAEMOSPORIDIA

605

after the bites of infected mosquitoes, but in one case as long as 304 days; in P. malariae, 4-5 weeks, with the onset of fever lagging 3-12

days behind; and in two strains of P. falciparum, one, 6-25 days and the other, 9-13 days; in another observation, P. falciparum was observable in the peripheral blood in 5-9 days and the onset of fever in 7-12 days.

The paroxysm of malaria is

usually divisible into three stages:

stage.

chill

or rigor stage, high temperature or febrile stage (104 F. or over)

and sweating or defervescent

zoites

The time

of

paroxysm

corre-

sponds, as was stated already, with the time of liberation of mero-

from erythrocytes, and

is

believed to be due to extrusion of

The nature of this mahowever unknown at present. In the grown schizonts as well as in gametocytes of Plasmodium, are fcund invariably yellowish brown to black pigment granules which vary in form, size and number among different species. They are usually called haemozoin granules and are apparently the catabolic products formed within the parasites. The pigment of P. gallinaceum and P. cynomolgi has been identified with haematin (ferri protoporphyrin) (Rimington and Fulton, 1947). The pigment possesses certain taxonomic significance,
certain substance into the blood plasma.
terial is

as will be described below.

The

infected erythrocytes,

if

stained

deeply,

may show

a punctate appearance. These dots are small

numerous
are
fected

in the erythrocytes infected

by P.

vivax

and P.

ovale,

and and

known as Schiiffner's (1899) dots, while those in the host cells inby P. falciparum are few and coarse and are referred to as Maurer's (1902) dots. No clots occur in the erythrocytes infected by
P. malariae. Pathology (Maegraith, 1948); splenomegaly (Darling,
1924, 1926; Russell, 1935, 1952a; Hackett, 1944); histopathology

and Mulligan, 1937); character of paroxysm (Kitchen and Putnam, 1946) blood proteins during infection (Boyd and Proske, 1941); stippling of erythrocytes (Thomson, 1928). The condition which brings about the formation of gametocytes is not known at present. The gametocytes appear in the peripheral blood at various intervals after onset of fever, and remain inactive while in the human blood. The assumption that the macrogametocytes undergo parthenogenesis under certain conditions and develop into schizonts as advocated by Grassi, Schaudinn and others, does not seem to be supported by factual evidence. The initiation of further development appears to be correlated with a lower temperature and also a change in pH of the medium (Man well). If living mature microgametocytes of human Plasmodium taken from an infected person are examined microscopically under a sealed cover glass
(Taliaferro
;

606
at

PROTOZOOLOGY
in

room temperature (18-22C), development takes place

a short

while and motile microgametes are produced ("exflagellation").

Similar changes take place

when the gametocytes

are taken into

the stomach of mosquitoes belonging to genera other than Anopheles,

but no sexual fusion between gametes occurs in them and all degenerate sooner or later. In the stomach of an anopheline mosquito, however, the sexual reproduction of human Plasmodium continues, as has been stated before. All species are transmitted by adult female mosquitoes. The males are not concerned, since they do not take blood meal. The species of Plasmodium which attack man are transmitted only by the mosquitoes placed in genus Anopheles, while the majority of the avian species of Plasmodium are transmitted by those which belong to genera
Culex, Aedes, and Theobaldia.
larial parasites in

The chief vectors of the human maNorth America are A. quadrimaculatus (eastern,

southern and middle-western States), A. punctipennis (widely distributed), A. crucians (southern and south-eastern coastal area), A.
walkeri (eastern area)
,

and

.4

Boyd and coworkers observed

maculipennis freeborni (Pacific coast) that (1) A. quadrimaculatus and A.

punctipennis were about equally susceptible to Plasmodium vivax;

(2) A. quadrimaculatus was susceptible to several strains of P. falciparum, while A. punctipennis varied from highly susceptible to refractory to the same strains; (3) A. quadrimaculatus was more susceptible to all three species of Plasmodium than coastal or inland A. crucians. Thus A. quadrimaculatus is the most dangerous malaria vector in the United States as it shows high susceptibility to all human Plasmodium. A. pseudopunctipennis distributed from southwestern United States to Argentina and A. albimanus occurring in Central America, are but a few out of many anopheline vectors of

human Plasmodium

in the areas indicated. Host-parasite relation

(Boyd and Coggeshall, 1938); malaria vectors of the world (Komp, 1948); susceptibility of Anopheles to malaria (King, 1916; Boyd and Kitchen, 1936); epidemiology in North America (Boyd, 1941), in Brazil (Boyd, 1926), in Jamaica (Boyd and Aris, 1929), in Cuba (Carr and Hill, 1942), in Trinidad and British West Indies (Downs, Gillette and Shannon, 1943), in Porto Rico (Earle, 1930, 1939), in Haiti (Paul and Bellerive, 1947), in Philippine Islands (Russell, 1934, 1935a), in India (Russell and Jacob, 1942) and in Liberia; general picture (Russell, 1952, 1952a); mosquito control (Russell, 1952a)

The time required for completion of sexual reproduction of Plasmodium in mosquitoes varies according to various conditions such
as species

and strain differences

in

both Plasmodium and Anopheles,

HAEMOSPORIDIA
temperature,
feed
etc.

607

phelines which fed on patients infected

after infective feeding,

Boyd and co-workers showed that when the anoby P. vivax were allowed to

on other persons, their infectivity was as follows: 1-10 days 87.2%; 11-20 days, 93.8%; 21-30 days, 78%; 31-40 days, 66%; 41-50 days, 20%; and over 50 days, none. In a
similar experiment with P. falciparum, during the
infection rate
first

10 days the

was 84%, but thereafter the infectivity rapidly diminished until there was no infection after 40 days. It is generally known that the development of the parasites in mosquitoes depends a great deal on temperature. Although the organisms may survive
mosquitoes (Coggeshall), sporozoite-formation is said not to take place at temperatures below 16 C. or above 35 C. (James). According to Stratman-Thomas (1940), the development of Plasmodium vivax in Anopheles quadrimaculatus is completed within the temperature range of 15-17 to 30 C. It varies from 8 to 38 days after infective feeding. The optimum temperature is said to be 28 C. at which the development is completed in the shortest time. A period of 24 hours at 37.5 C. will sterilize all but a very small per cent of Anopheles quadrimaculatus of their Plasmodium vivax infection. This has a bearing on the transmission of Plasmodium vivax in summer months. In certain localities oocysts may survive the winter and complete their development in the following spring. Duration of infection in Anopheles (Boyd and St.-Thomas, 1943a; Boyd, St.-Thomas and Kitchen, 1936). There are three long-recognized species of human Plasmodium. They are P. vivax, P. falciparum and P. malariae. To these P. ovale is here added. Each species appears to be represented by numerous strains or races as judged by the differences in virulence, immunological responses, incubation period, susceptibility to quinine, etc.

freezing temperature in

(Boyd, 1934, 1940, 1940a; Boyd and Kitchen, 1948). Malaria has been, and still is, perhaps the most important protozoan disease of man. In India alone, malaria fever is held to be the direct cause of over a million deaths annually among nearly 100 million persons who suffer from it (Sinton, 1936). In the United States, the disease had been prevalent in places in south-eastern States. But since 1945, cases of malaria have rapidly declined and there is prospect of the disappearance of endemic malaria from the United States (Andrews, Quinby and Langmuir, 1950; Andrews, 1951). In malarious countries, the disease is a serious economic and social problem, since it affects the majority of population and brings about a large number of persistent sickness, the loss of man power and retardation of both mental and physical development among

608
children.

PROTOZOOLOGY
History of malaria (Ross,
1928; Boyd, 1941; Russell,

1943); general reference (Boyd, 1949; Russell,

West and Manwell,

1946); antimalarial drugs (Russell, 1952a).

It must be added here that human ingenuity has been for nearly 30 years utilizing the malarial organisms in combating another disease; namely, naturally induced malaria therapy has been successfully used in the treatment of patients suffering from general paresis

r t+f t

Fig. 259.
b, c,

Plasmodium

vivax,
d,

X1535
j,

(Original),
in

a,

young ring-form;
e,
f,

growing schizonts;
1,

two schizonts
fully

an erythrocyte;

large

schizonts; g-i, schizogonic stages;

developed merozoites;

k,

macro-

gametocyte;

microgametocyte.

and other forms of neuro-syphilis. Technique (Boyd and StratmanThomas, 1933; Boyd, St.-Thomas and Kitchen, 1936a; Boyd, St.Thomas, Kitchen and Kupper, 1938; Mayne and Young, 1941). P. vivax (Grassi and Feletti) (Fig. 259). The benign tertian malaria parasite; schizogony completed in 48 hours and paroxysm every third day. Ring forms: About 1/4-1/3 the diameter of erythrocytes; unevenly narrow cytoplasmic ring is stained light blue (in Giemsa) and encloses a vacuole; nucleus stained dark-red, conspicuous. Growth period: Irregular amoeboid forms; host cell slightly enlarged; Schuffner's dots begin to appear. Grown schizonts: In about 26 hours after paroxysm; occupy about 2/3 of the enlarged erythrocytes, up to 12^ in diameter, which are distinctly paler than uninfected ones; Schuffner's dots more numerous; brownish haemozoin granules; a large nucleus. Schizogonic stages: Repeated nuclear division produces

HAEMOSPORIDIA

609

12-24 or more merozoites; multinucleate schizonts about 8-9m in diameter; haemozoin granules in loose masses; merozoites about 1.5m

Time required for development of ringform into a mature gametocyte is estimated to be about four days; smoothly rounded body, occupying almost whole of the enlarged erythrocytes; brown haemozoin granules numerous. Macrogametocytes are about 9-10/j. in diameter, stain more deeply and contain a small compact nucleus; microgametocytes are a little smaller (7-8/x in diameter), stain less deeply and contain a less deeply staining large nucleus. This species is said to invade reticulocytes rather than erythrocytes
long. Gametocytes:

(Kitchen, 1938).

Boyd

(1953a) distinguished five series of erythro-

>
e
Fig. 260.
f

Plasmodium falciparum, X1535 (Original), a, three ring-forms in an erythrocyte; b, a somewhat grown schizont in an erythrocyte with Maurer's dots; c-f, growing and schizogonic stages, g, h; merozoite formation; i, macrogametocyte; j, microgametocyte.
cytic organisms on the basis of nuclear
istics.

and cytoplasmic characterorganisms

series

The organisms

of series

A give rise by schizogony to

C
of infection
is

of series

or

or series

produce (macrogametocytes). Onset

in turn

which

(microgametocytes)
said to occur

3 (Boyd, than 100 per 1944). Incubation period (Boyd and Stratman-Thomas, 1933c, 1934) concentration of organisms (Ferrebee and Geiman, 1946) immunity (Boyd and Stratman-Thomas, 1933a, b; Boyd and Kitchen, 1936a; Boyd, 1947); susceptibility (Boyd and Stratman-Thomas,

usually

when the

parasite density

is

less

mm

1933c, 1934).

The benign malaria fever parasite is the commonest and the most widely distributed species in the tropical and subtropical regions as well as in the temperate zone. It has been reported as far north as the
Great Lakes region in North Ameria; England, southern Sweden and northern Russia in Europe; and as far south as Argentina, Australia, and Natal in the southern hemisphere. Generally speaking this spe-

610
cies

PROTOZOOLOGY
predominates in the spring and early summer over the other

species.

P. falciparum (Welch) {Laverania malariae Grassi and Feletti; P.

The subtertian, malignant tertian or aestivo-autumnal fever parasite; schizogonic cycle is somewhat irregular, though generally about 48 hours. Ring forms: Much smaller than those of P. vivax; about In in diameter; marginal forms and multiple (2-6) infection common nucleus often rod-form or divided into two granules; in about 12 hours after paroxysm, all schizonts disappear from the peripheral blood. Growth and schizogonic stages: These are almost exclusively found in the capillaries of internal organs; as schizonts mature, Maurer's dots appear in the infected erythrocytes; when about 5/x in diameter, nucleus divides repeatedly and 8-24 or more small merozoites are produced; haemozoin granules dark brown or black and usually in a compact mass; infected erythrocytes are not enlarged. Gametocytes: Mature forms sausage-shaped ("crescent"), about 10-12ju by 2-3ju; appear in the peripheral blood. Macrogametocytes stain blue and contain a compact nucleus and coarser granules, grouped around nucleus; micro gametocytes stain less deeply blue or reddish, and contain a large lightly staining nucleus and scattered smaller haemozoin granules. The organism invades both mature and immature erythrocytes (Kitchen, 1939). Cytological study of microgametocytes and microgametes (MacDougall, 1947) different strains (Kitchen and Putnam, 1943); induced infection (Boyd and Kitchen, 1937); incubation period (Boyd and Kitchen, 1937b; Boyd and Matthews, 1939); immunity (Boyd and Kitchen, 1945).
tenue Stepens) (Fig. 260).
; ;

The subtertian

fever parasite
it is

is

widely distributed
in late

in the tropics.

In the subtropical region,

more prevalent

autumn. It is relatively uncommon in the malignancy of the fever brought about by this parasite

summer or early temperate zone. The

is

attributed

in part to decreased elasticity of the infected erythrocytes

which be-

come clumped together

into masses

and which adhere

to the walls of

the capillaries of internal organs especially brain, thus preventing the

circulation of blood through these capillaries.

P. malariae (Laveran) (Fig. 261). The quartan malaria parasite; schizogony in 72 hours and paroxysm every fourth day. Ring forms: Similar to those of P. vivax. Growth period: Less amoeboid, rounded; in about 6-10 hours haemozoin granules begin to appear; granules
are dark brown; in 24 hours, schizonts are about 1/2 the diameter
of

erythrocytes which

remain normal

in

size;

schizonts

often

stretched into "band-form" across the erythrocytes; no dots com-

parable with Schiiffner's or Maurer's dots. Mature and segmenting

HAEMOSPORIDIA
schizonts: In

611

about 48 hours, schizonts nearly fill the host cells; rounded; haemozoin granules begin to collect into a mass; nuclear divisions produce 6-12 merozoites which are the largest of the three species and may often be arranged in a circle around a haemozoin
mass. Gametocytes : Circular; with haemozoin granules. Macrogametocytes stain more deeply and contain a small, more deeply staining

#
i

Fig. 261.

Plasmodium malariae, X1535

(Original), a, ring-form;
j,

b-e,
k.

band-form schizonts; f-i, schizogonic stages; macrogametocyte, 1, microgametocyte.

merozoite formation;

nucleus and coarser granules; microgametocytes stain less deeply and contain a larger lightly stained nucleus and finer and numerous granules. The organism invades most frequently mature red corpuscles (Kitchen, 1939).

The quartan
tropics,

fever parasite

is

distributed in the tropics

and sub-

though it is the least common of the three species. As a rule, in an area where the three species of Plasmodium occur, this species seems to appear later in the year than the other two. P. ovale Stevens (Fig. 262). The Ovale or mild tertian fever parasite; schizogony in about 48 hours; its morphological characters resemble both P. vivax and P. malariae. Ring forms: Similar to those of the two species just mentioned; Schiiffner's dots appear
early.

Growth period: Infected erythrocytes are more or less oval with irregular fimbriated margin; slightly enlarged; not actively amoeboid, sometimes in band-form; with dark brown haemozoin

612

PROTOZOOLOGY
Gametocytes: Resemble closely those of P. malariae; host
cells

granules; Schuffner's dots abundant. Schizogonic stages: 6-12 merozoites.

with Schuffner's dots and slightly enlarged. This organism appears to be confined to Africa and Asia (Philippine Islands and India). Several malariologists doubt the validity of
the species.

The
three

malarial parasites are ordinarily studied in stained blood

films (p. 899).

Table
species.

11 will serve for differential diagnosis of the

common

'r%

e
Fig. 262.

g
ovale,

h
a,

Plasmodium

X1535

(Original),

growing schizonts; gametocyte.

d-f, schizogonic stages; g,

ring-form; b, c, macrogametocyte; h. micro-

Several species of Plasmodium have been observed in primates and monkeys, some of which resemble strikingly the human species. Here a few species will be mentioned. Other species (Aberle, 1945).

P. kochi (Laveran) (Fig. 263, a-f). In the

monkeys belonging

to

the genera: Callicebus, Cercocebus, Cercopithecus, Erythrocebus,

fected erythrocytes

and Papio; schizogony in 48 hours; organism resembles P. vivax; inbecome enlarged and sometimes stippling like
Schuffner's dots occurs; eight to 14 merozoites; gametocytes large

and spheroid.
P. brasilianum Gonder and Berenberg-Gossler (Fig. 263, g-l). In

New World monkeys

belonging to the genera: Alouatta, Ateles,

Cacajao and Cebus; schizogony in 72 hours; it resembles P. malariae; no enlargement of infected erythrocytes; band-form schizonts; number of merozoites vary according to the difference in hosts, averaging eight to 10; gametocytes rounded, comparatively small in

number
and

(Taliaferro

and

Taliaferro, 1934).

Haematology

(Taliaferro

Kliiver, 1940).

P. cynomolgi

Mayer

(Fig. 263, m-r). In

Macaca

irus

(Macacus


HAEMOSPORIDIA
Table
11.

613

Differential diagnosis of three species of

human Plasmodium

614

PROTOZOOLOGY

feiy

w?

iit*

Fig. 263. Plasmodium of monkeys. Column 1, ring forms; 2, 3, growing trophozoites; 4, segmenting schizonts; 5, macrogametocytes; 6, micro-

gametocytes.

a-f,

Plasmodium

kochi,

X1665 (Gonder and BerenbergX2000;

s-x, P.

Gossler); g-1, P. brasilianum, X1665; m-r, P. cynomolgi, knowlesi, X2000 CTaliaferro and Taliaferro).

P. knowlesi Sinton and Mulligan (Fig. 263, s-x). In

Macaca

irus;

experimentally

man

is

susceptible; schizogonic cycle in 24 hours; six

somewhat distorted. Morphology and development (Brug, 1934; Mulligan, 1935; Taliaferro and Taliaferro, 1949); infections in man (Milam and Coggeto 16 merozoites; infected erythrocytes are
shall, 1938).

of

P. berghei Vincke and Lips. In the tree rat, Thamnomys surdaster Congo (Vincke and Lips, 1948). White mice, white rats, cotton
the field vole (Microtus guntheri) and the golden hamster

rats,

{Mesocricetus auratus) are susceptible; mosquito vector, Anopheles

dureni (Mercado and Coatney, 1951).

Plasmodium have been reported from numerous which are observed clinical symptoms and pathlogical changes similar to those which exist in man with malaria infection. In recent years the exoerythrocytic stages have been intensively studied in these forms. According to Hegner and cospecies of species of birds in

Many

HAEMOSPORIDIA

615

workers the erythrocytes into which merozoites enter are often the most immature erythrocytes (polychromatophilic erythroblasts). The species of avian Plasmodium are transmitted by adult female mosquitoes belonging to Culex, Aedes or Theobaldia. Some of the

common

species are briefly

mentioned here. Avian Plasmodium

(Manwell, 1935a; Hewitt, 1940b); avian hosts (Wolfson, 1941); distribution (Man well and Herman, 1935; Herman, 1938; Hewitt,
1940a;

Wood and Herman,

(Fig. 264, a).

1943).
;

P. relictum Grassi and Feletti (P. praecox G. and F.

P. inconstans

Hartman)

In English sparrow (Passer domesticus) and other passerine birds, also in mourning doves and pigeons (Coatney 1938); schizogony varies in different strains, in 12, 24, 30 or 36 hours; 8-15 or 16-32 merozoites from a schizont; gametocytes
rounded, with small pigment granules; host-cell nucleus displaced; canaries (Serinus canaria) susceptible; many strains; transmitted by
tion

Culex, Aedes and Theobaldia; widely distributed. Duration of infec(Manwell, 1934; Bishop, Tate and Thorpe, 1938); variety

(Manwell, 1940);
birds

in

(Mudrow and Reichenow,

Culex pipieris (Huff, 1934); development in 1944); relationship of E.-E. and

erythrocytic stages (Sergent, 1949).

P. vaughani Novy and McNeal (Fig. 264, b). In robin (Turdus m. migratorius) and starling (Sturnus v. vulgaris) 4-8 (usually 4) merozoites from a schizont, ordinarily with 2 pigment granules; schizogony in about 24 hours; gametocytes elongate; host-cell nu;

cleus not displaced.

bird,

Hartman (Fig. 264, c). In English sparrow, cowred-winged blackbird, and other birds; schizogony in 24 hours, segmentation occurs at 6-10 p.m.; 6-24 merozoites from a schizont; mature schizonts and gametocytes about 7-8ju in diameter; gametocytes rounded; haemozoin granules in microgametocytes longer and
P. cathemerium

more pointed than those present in macrogametocytes; canaries susceptible; numerous strains; common; transmitted by many species of Culex and Aedes (Hartman, 1927). Relapse (Manwell, 1929); acquired immunity (Cannon and Taliaferro, 1931) in ducks (Hegner and West, 1941); cultivation (Hewitt, 1939); effect of plasmochin
;

(Wampler, 1930).
P. rouxi Sergent, Sergent and Catanei (Fig. 264, d). In English sparrow in Algeria; similar to P. vaughani; schizogony in 24 hours; 4 merozoites from a schizont; transmitted by Culex. P. elongatum Huff (Fig. 264, e). In English sparrow; schizogony occurs mainly in the bone marrow, and completed in 24 hours; 8-12 merozoites from a schizont; gametocytes elongate, found in periph-

616
eral blood; transmitted

PROTOZOOLOGY
by Culex
(Huff, 1930). Canaries

and ducks

are susceptible. Study of nucleus (Chen, 1944).

P. circumflexum Kikuth (Fig. 264,/). In the red-winged blackbird, cowbird and several other birds, including the ruffed grouse (Fallis, 1946) growing schizonts and gametocytes form broken rings around
;

is

(o)8

d,

Fig. 264. a, Plasmodium rdictum; b, P. vaughani; c, P. cathemerium; P. rouxi; e, P. elongatum; f, P. circumflexum; g, P. polare; h, P. nucleophilum; i, P. gallinaceum; j, P. hexamerium; k, P. oti; 1, P. lophurae. Columns 1, ring-forms; 2, growing schizonts; 3, segmenting schizonts; 4, macrogametocytes; and 5, microgametocytes. X about 1400 (Several authors; from Hewitt, modified).

HAEMOSPORIDIA

617

the host-cell nucleus; schizogony in 48 hours; 13-30 merozoites;

gametocytes elongate, with a few haemozoin granules; transmission by Theobaldia (Herman, 1938b). P. polare Manwell (Fig. 264, g). In cliff swallow (Petrochelidon I. lunifrons) grown schizonts at one of the poles of host erythrocytes; 8-14 merozoites from a schizont; few in peripheral blood; gametocytes elongate (Manwell, 1935a). P. nucleophilum M. (Fig. 264, h). In catbird (Dumatella carolinensis); schizogony in 24 hours; 3-10 merozoites from a schizont; mature schizonts usually not seen in the peripheral blood; gameto;

cytes elongate, often seen closely applied to the host-cell nucleus;

haemozoin granules at one end (Manwell, 1935a).

P. gallinaceum

Brumpt

(Fig. 264,

i).

In domestic fowl (Gallus

domesticus) in India; schizogony in 36 hours; 20-36 merozoites from a

schizont; gametocytes round, with few haemozoin granules; host-cell

nucleus displaced; pheasants, geese, partridges and peacocks are

susceptible, but canaries, ducks, guinea fowls, etc., are refractory;

transmitted by Aedes (Brumpt, 1935). E.-E. development

vectors (Russell and

(p.

602);

Mohan,

1942); phosphorus 32 in study (Clarke,

1952); nucleic acids (Lewert, 1952).

Maryland yellow-throats; schizogony

elongate (Huff, 1935). P.
oti
;

P. hexamerium Huff (Fig. 264,,/). In bluebird (Sialias. sialis) and in 48 or 72 hours; grown schi-

zonts often elongate; 6 merozoites from a schizont; gametocytes

Wo If son

(Fig. 264, k). In eastern screech

;

owl (Otus asio

naevius) 8 merozoites from a schizont

body outlines irregular, rough

gametocytes elongate. Manwell (1949) considers this species identical with P. hexamerium. P. lophurae Coggeshall (Fig. 264, 1). In fire-back pheasant (Lophura i. igniti) from Borneo, examined at New York Zoological Park; 8-18 merozoites from a schizont; gametocytes large, elongate; hostcell nucleus not displaced; canaries are refractory, but chicks and especially ducks are highly susceptible (Coggeshall, 1938, 1941; Wolfson, 1940) young ducklings succumb less readily to its infection than older ducks (Becker, 1950). Experimentally Aedes aegypti, A. albopictus and Anopheles qvadrimaculatus serve as vectors, but not Culex pipiens (Jeffery, 1944). Characteristics (Terzian, 1941); culti;

vation (Trager, 1950).

A number of lizards have recently been found to be infected by Plasmodium. A few species are described here briefly. Species (Thompson and Huff, 1944a; Laird, 1951). P. mexicanum Thompson and Huff (Fig. 265). In Sceloporus fer-

618
rariperezi of

PROTOZOOLOGY

Mexico; experimentally S. olivaceous, S. undulatus, Crotaphytus collaris, PhrynQsoma cornutum and P. asio, become in;

fected in erythrocytes

and normoblasts, and

;

in all types of circulat-

ing cells; host cells not hypertrophied

schizonts round to elongate;

ju,

10-40 merozoites; gametocytes 12-16/z by 6-7.

only in haemo-

globin-containing cells which become enlarged and distorted

(Thomp-

son and Huff, 1944); a mite, Hirstella sp., was considered to be a possible vector (Pelaez, Reyes and Barrera, 1948).

Fig. 265. Plasmodium mexicanum, X1780 (Pelaez et al. ). a, b, young and growing trophozoites in host's erythrocyte; c, segmenting schizont; d, macrogametocyte; e, microgametocyte.

P. rhadinurum T. and H. In the erythrocytes of Iguana iguana

rhinolopha in Mexico; schizonts extremely polymorphic with one or

two long processes; 4-5 merozoites; gametocytes 6. 5-7. In vector unknown (Thompson and Huff, 1944a). P.floridense T. and H. In the erythrocytes of Sceloporus undulatus in Florida; young trophozoites pyriform; 6-21(12) merozoites; gametocytes 7.5-8.0/u in diameter; vector unknown (Thompson and
;

Huff, 1944a)

P. lygosomae Laird. In
1951).

New Zealand skink,

Lygosoma moco (Laird,

Family 2 Haemoproteidae Doflein

Schizogony occurs in the endothelial cells of vertebrates; merozoites enter circulating blood cells and develop into gametocytes; if blood is taken up by specific blood-sucking insects, gametocytes develop into gametes which unite to form zygotes that undergo changes similar to those stated above for the family Plasmodiidae. Genus Haemoproteus Kruse. Gametocytes in erythrocytes, with pigment granules, halter-shaped when fully formed (hence Halteridium Labbe) schizogony in endothelial cells of viscera of vertebrate
;

reptiles.

Species (Cerny,

transmission experiments (Noller,

1933; Coatney and Roudabush, 1 Q 20).

1937);

HAEMOSPORIDIA
H. columbae
livid), etc.;

619

Celli and Sanfelice (Fig. 266). In pigeons (Columba widely distributed; young schizonts, minute and uninucleate, are in the endothelial cells of lungs and other organs, grow into large multinucleate bodies which divide into 15 or more uninucleate cytomeres (Aragao). Each cytomere now grows and its nucleus

The host cell in which many cytomeres undergo enlargement, becomes highly hypertrophied and finally ruptures. The multinucleate cytomeres break up into numerous merozoites,
divides repeatedly.

which possibly repeat the schizogony by invading endothewhile others enter erythrocytes and develop into gametocytes which are seen in the peripheral blood; sexual reproduction

some

of

lial cells,

Fig. 266. The life-cycle of Haemoproieus columbae. (Several authors), a sporozoite entering an endothelial cell of the pigeon; b, growth of a schizont; c, segmentation of multinucleate schizont into uninucleate
a,

cytomeres; d-i, development of cytomeres to produce merozoites; j-m, development of microgametes; n-p, development of macrogamete; q, fertilization; r, s, ookinetes; t, a young oocyst in the stomach wall of a fly; u, a ruptured mature oocyst with sporozoites. a-k, n, o, in the pigeon, 1, m, p-u, in Pseudolynchia maura.

620
in,

PROTOZOOLOGY
and transmitted by, the
flies:

Lynchia brunea, L.

lividicolor, L.

capensis, Pseudolynchia maura,

and Microlynchia fusilla. Nomencla-

ture and relapse (Coatney, 1933).

H. lophortyx O'Roke. In California valley quail, Gambel quail, and Catalina Island quail (Lophortyx) gametocytes in erythrocytes, also occasionally in leucocytes; young gametocytes, spherical to elongate, about 1m long; more developed forms, cylindrical, about 8m by 2m, with 2-10 pigment granules; mature gametocytes, haltershaped, encircling the nucleus of the host erythrocyte, 18m by 1.52.5m; numerous pigment granules; 4-8 microgametes, about 13. 5m long, from each microgametocyte; on slide in one instance, gameteformation, fertilization and ookinete formation, completed in 52
;

minutes at room temperature; in nature sexual reproduction takes place in the fly, Lynchia hirsuta; sporozoites enter salivary glands and fill central tubules; schizonts present in lungs, liver and spleen of quail after infected flies sucked blood from the bird; merozoites found in endothelial cells of capillaries of lungs, in epithelial cells of liver and rarely in peripheral blood cells; how merozoites enter blood cells is unknown; schizonts seldom seen in circulating blood; infected birds show pigment deposits in spleen and lungs (O'Roke, 1934). Duration of infection (Herman and Bischoff, 1949). H. metchnikovi (Simond). In the Indian river tortoise, Trionyx indicus and the yellow-bellied terrapin, Pseudemys elegans (Hewitt,
1940).

Genus Leucocytozoon Danilewsky. Schizogony

cells

in the endothelial

as well as visceral cells of vertebrates; sexual reproduction in

blood-sucking insects; gametocytes in spindle-shaped host cells. Several species (Cerny, 1933; Coatney and Roudabush, 1937). L. simondi Mathis and Leger (L. anatis Wickware) (Fig. 267). Mathis and Leger (1910) described this species from the teal duck (Querquedula crecca) in Tonkin, China. Wickware (1915) saw L.

O'Roke (1934) carried on experimental on the developmental cycle with the form which he found in wild and domestic ducks in Michigan. Herman (1938) observed the organism in common black ducks (Anas rubripes tristis), red-breasted merganser (Mergus serrator), and blue-winged teal (Querquedula discors) and considered L. anatis as identical with L. simondi. Huff (1942) studied the schizogony and gametocytes, and maintained the species he studied in mallard ducks (Anas p. platyrhynchos) and domestic ducks from Wisconsin, to be L. simondi. According to O'Roke, the vector is the black fly, Simulium venustum, in which the sexual reproduction takes place. Gametocytes deanatis in ducks in Canada.

studies

HAEMOSPORIDIA

621

velop into mature gametes in 1-2 minutes after blood is obtained from an infected duck; macrogametes about 8ju in diameter; 4-8 microgametes, 15.7-24. In long, from a single microgametocyte; zygotes are found in stomach contents of fly in 10-20 minutes after sucking

Fig. 267.
a-c,

The

life-cycle of Leucocytozoon

development

of

macrogamete;
i,

g, fertilization; h,

ookinete;

j,

simondi (Brumpt, modified), development of microgametes; ookinete piercing through the stomach
d-f,

wall;

k-m, development

of sporozoites; n, sporozoites entering endo-

thelial cells; o-r, schizogony.

blood of bird motile ookinetes abundant after 5 hours, measure 33. 3m by 3-4.6^; 22 hours after sucking duck blood, oocysts are found on outer wall of stomach; sporozoites mature probably in 24-48 hours; 5 days after a duck has been bitten by infected black
in the infected
;

flies,

of lungs, liver, spleen;

liver

schizogonic stages are noticed in endothelial cells of capillaries on about 7th day gametocytes appear in blood

and spleen become hypertrophied the infection among duck;

622
lings
is

PROTOZOOLOGY
said to be highly fatal

and appears often suddenly. In addiSimulium mentioned above, Simulium parnassum appears to be a vector (Fallis, Davies and Vickers, 1951). Mathis and Leger: Macrogametocytes, oval; 14-15/x by 4.5-5.5/*;
tion to the

several vacuoles in darkly stained cytoplasm. Microgametocytes,

oval; slightly smaller; cytoplasm stains less deeply. Infected host

about 48/* long; nucleus elongate. Huff found that (1) young schizonts are in macrophages of, and also extracellularly in, the spleen and liver; (2) two types of schizonts occur: one, "hepatic schizonts" in hepatic cells which cause no distortion or alteration of the host cell, and the other, "megalocells

schizonts" in the blood vessels

spleen, liver

of,

or extravascularly

in,

the heart,

become divided into many cytomeres which give rise to numerous merozoites; (4) young gametocytes occur in lymphocytes, monocytes, myelocytes and late polychromatophile ery throblasts (5) the cells in which fully grown gametocytes occur, appear to be macrophages. Life history and effect on the blood of host birds (Fallis, Davies and Vickers, 1951); deintestine; (3) megaloschizonts
;

and

velopment in ducklings (Chernin, 1952). Other reported species: L. smithi Laveran and Lucet (1905)

in

turkey; L. bonasae Clarke (1935) in ruffed grouse; L. andrewsi Atchley (1951) in chicken, etc.

Family 3 Babesiidae Poche

Minute non-pigmented parasites of the erythrocytes of various mammals; transmission by ticks. Genus Babesia Starcovici (Piroplasma Patton). In erythrocytes of
arranged in couples; sexual reproduction in fewhich developing ova, hence young ticks, become infected with ookinetes, producing sporozoites which enter salivary
cattle; pear-shaped,

male

ticks in

glands (Dennis).

Taxonomy

(Toit, 1918).

B. bigemina (Smith and Kilborne) (Figs. 268; 269, a-d). The causative organism of the haemoglobinuric fever, Texas fever or

red-water fever of cattle; the very first demonstration that an arthropod plays an important role in the transmission of a protozoan
parasite; the infected cattle contain in their erythrocytes oval or

the division

pyriform bodies with a compact nucleus and vacuolated cytoplasm; is peculiar in that it appears as a budding process at the beginning. We owe Dennis (1932) for our knowledge of the development of the organism.
Sexual reproduction followed by sporozoite formation occurs in
the tick, Boophilus (Margaropus) annulatus;

when a

tick takes in

HAEMOSPORIDIA
infected blood into gut lumen, isogametes, 5.5-6> long, are produced;

isogamy results in motile club-shaped ookinetes, 7- 12m long, which pass through gut wall and invade larger ova (1-2, in one case about 50, ookinetes per egg) each ookinete rounds itself up into a sporont 7.5-12m in diameter, which grows in size and whose nucleus divides repeatedly; thus are produced multinucleated (4-32 nuclei) amoeboid sporokinetes, up to 15m long, which now migrate throughout
;

Fig. 268. The life-cycle of Babesia bigemina (Dennis), a-f, division in erythrocytes of cattle; g, h, gametocytes; i, isogametes; j, fertilization; k, zygote; 1, ookinete penetrating through the gut wall; m, ookinete in host egg; n-p, sporoblast-formation; q, sporokinetes in a large embryonic cell; r, sporozoites in salivary gland.

624

PROTOZOOLOGY
cells of tick,

embryonic tissue

many

of which cells develop into

salivary gland cells; sporokinetes develop into sporozoites before or

after hatching of host tick; sporozoites bring about
cattle

when they

are inoculated

by

tick at the time of feeding.

an infection to Texas
to the cattle

fever once caused a considerable

tion of the tick
limited.

amount

of

damage

industry in the southern United States to which region the distribuis

Rees (1934) maintains that there

species, B. argentina Lignieres.

is

in

addition a

somewhat smaller

Fig. 269. a-d, Babesia bigemina, X3Q00 (Nuttall); e-h, B. bovis, X3000 (Nuttall); i-1, Theileria parva, X3000 (Nuttall); m-s, Dactylosoma ranarum (m-q, schizogony; r, s, gametocytes), X2700 (Noller).

B. bovis Starcovici (Fig. 269, e-h). In European cattle; amoeboid form usually rounded, though sometimes stretched; 1-1. 5m in diameter; paired pyriform bodies make a larger angle, 1.5-2/* long;

transmitted by Ixodes ricinus.

B. canis (Piana and Galli-Valerio). Pyriform bodies 4.5-5/x long;

the organism causes malignant jaundice in dogs; widely distributed;

transmitted by the ticks: Haemaphysalis

guineus,
1933).

leachi,

Rhipicephalus san-

and Dermacentor

reticulatus

(Regendanz and Reichenow,

HAKMOSPORIDIA

025

Species of Babesia occur also in sheep, goats, pigs and horses.

Genus Theileria Bettencourt, Franga and Borges. Schizogony

takes place in endothelial cells of capillaries of viscera of mammals; certain forms thus produced enter erythrocytes and appear in

the peripheral circulation. T. parva (Theiler) (Fig. 269, i-l). In the cattle in Africa, cause of African coast fever; intracorpuscular forms 1-2/z in diameter; trans-

mitted by the tick, Rhipicephalus evertsi and R. appendiculatus (Reichenow, 1937). Genus Dactylosoma Labbe. In blood of reptiles and amphibians; schizogony and gametocytes in erythrocytes; invertebrate hosts

unknown. D. ranarum (Kruse)

(Fig. 269, ra-s). In European frogs; schizonts 4-9m in diameter; 4-16 merozoites, 2-3m by 1-1. 5/x; gametocytes 5-8m by 1.5-3m. Genus Toxoplasma Nicolle and Manceaux. Minute intracellular

and endothelial cells of various mammals, round or ovoid; usually not common in peripheral blood, though infective through inoculation; ordinarily abundant in the liver, spleen, bone marrow, lung, brain, etc.; multiplication by binary fission (Nicolle and Manceaux, 1909). Several species were designated by observers on the basis of the difference in host species. Taxonomy (Chatton and Blanc, 1917) morphology (Arantes 1914); relation to Plasmodium (Hegner and Wolfson, 1938; Manparasites in leucocytes
birds

and

reptiles;

well, 1939, 1941).

^0
Fig. 270. Toxoplasma gondii. X about 1750. (Chatton and Blanc) isolated organisms; b, 2 trophozoites; c, organisms undergoing binary fission; d, a host cell with many organisms which developed by repeated

a,

binary

fission.

T. gondii
in

N. and M. (Fig. 270). In Ctenodactylus gundi, a rodent North Africa; a variety of experimental animals susceptible to it;

crescentic; 4-6m

by 2-3m;

division occurs intra- or extra-cellularly.

626

PROTOZOOLOGY
rats,

Since the subcutaneous tissues of experimentally infected animals

such as

pigeons and chicks do not harbor parasites in the ab-

sence of parasitemia and the organisms are apparently present in the blood, transmission may be carried on by blood-sucking arthropods

(Jacobs and Jones, 1950).

Toxoplasma appears to be common in birds. For example, in a survey on the blood parasites of birds on Cape Cod, Herman (1938) found the organism in 11 species of birds examined by him. In the past ten years a considerable amount of information has accumulated on the organisms which attack and produce a disease (toxoplasmosis) in man. References (Sabin, 1942; Schwarz, Rose and Fry,
1948; Mantz, Sailey and Grocott, 1949; Hogan, 1951;
1952).

Weinman,

References
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Aberle,

S.

Dissert., Coll.

Atchley, F.
483.

Med., Rio de Janeiro. O.: (1951) Leucocytozoon andrewsi, etc. J. Parasit., 37:

in relation to age in young white Pekin ducks with blood-induced Plasmodium lophurae infection. Proc. Iowa Acad. Sci., 57:435. Bishop, Ann, Tate, P. and Thorpe, Mary V.: (1938) The duration

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388.

Boyd, M.
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J.,

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(1935)

The comparative morphology

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69.

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An

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historical sketch of the prevalence of malaria in Ibid., 21 223.

:

HAEMOSPORIDIA

627

On Soc, immunity A A comprehensive from and W. A Am. Med., and Coggeshall, A resume Med. Mai, The and Kitchen,
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the parasite density prevailing at certain periods (1944) 3:159. vivax malaria infection. J. Nat. Mai. review of studies on to vivax malaria. (1947)

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69.

survey of all aspects of (1949) Malariology. a global standpoint. 2 vols. Philagroup of diseases delphia. malaria survey of the island of Aris, F. (1929) 9:309. J. Trop. Jamaica, B.W.I. L. T.: (1938) of studies on the host-parasite relation in malaria. Tr. 3rd Int. Congr. Trop. 2:292. comparative susceptibility S. F.: (1936) of Anopheles quadrimaculatus, etc. Am. J. Trop. Med., 16:67. (1936a) On the efficiency of the homologous properties of acquired immunity to Plasmodium vivax. Ibid., 16:447. (1937) Observations on induced falciparum malaria. Ibid., 17:213. consideration of the duration of the in(1937a) trinsic incubation period in vivax malaria, etc. Ibid., 17:437. (1937b) The duration of the intrinsic incubation period in falciparum malaria, etc. Ibid., 17:845. (1945) On the heterologous value of acquired immunity to Plasmodium falciparum. J. Nat. Mai. Soc, 4:301. (1948) On the homogeneity or heterogeneity of Plasmodium vivax infections acquired in highly endemic region. Am. J. Trop. Med., 28:29. and Matthews, C. B.: (1939) An observation on the incubation period of Plasmodium falciparum. Am. J. Trop. Med., 19:
this
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H. O.: (1941) Observations on the blood proteins during malaria infections. Ibid., 21:245.
K.: (1933) A controlled technique for the employment of naturally induced malaria in the therapy of paresis. Am. J. Hyg., 17:37. (1933a) Studies on benign tertian malaria. I. Ibid.,
17:55.

(1933b) III. Ibid., 18:482. (1933c) IV. Ibid., 18:485. - (1934) V. Ibid., 19:541. (1934a) On the duration of infectiousness in Anopheles harboring Plasmodium vivax. Ibid., 19:539. and Kitchen, S. F.: (1936) On the duration of infectiousness in Anopheles harboring P. falciparum. Am. J. Trop. Med., 16:157. (1936a) Modifications in a technique for the employment of naturally induced malaria in the therapy of paresis.

Ibid., 16:323.

results

and Kupper, W. H.: (1938) A review from the employment of malaria therapy in the

of the

treat-

628

PROTOZOOLOGY
ment
of neurosyphilis in the Florida State Hospital.

Am.

J.

Psychiatry, 94:1099. Brug, S. L.: (1934) Observations on monkey malaria. Revista Malaria, 13:121. Brumpt, E.: (1935) Paludisme aviaire: Plasmodium gallinaceum n. sp., de la poule domestique. C. R. Acad. Sc, 200:783. Cannon, P. R. and Taliaferro, W. H.: (1931) Acquired immunity in avian malaria. III. J. Prev. Med., 5:37. Carr, H. P. and Hill, R. B. (1942) A malaria survey of Cuba. Am. J. Trop. Med., 22:587. Cerny, W. (1933) Studien an einigen Blutprotozoen aus Vogeln. Arch. Protist., 81:318. Chatton, E. and Blanc, G.: (1917) Notes et reflexions sur le toxoplasme et la toxoplasmose du gondi. Arch, l'lnst. Pasteur, Tunis, 10:1. Chen, T. T.: (1944) The nuclei in avian malaria parasites. I. Am. J. Hyg., 40:26. Chernin, E.: (1952) Parasitemia in primary Leucocytozoon simondi infections. J. Parasit., 38:499. Clarke, C. H. D: (1938) Organisms of a malarial type in ruffed grouse, etc. J. Wildlife Manag., 2:146. Clarke, D. H.: (1952) The use of phosphorus 32 in studies on Plasmodium gallinaceum. I, II. J. Exper. Med., 96:439. Coatney, C. R. (1933) Relapse and associated phenomena in the Haemoproteus infection of the pigeon. Am. J. Hyg., 18: 133. (1938) A strain of Plasmodium relictum from doves and pigeons, etc. Ibid., 27:380. and Roudabush, R. L. (1937) Some blood parasites from Nebraska birds. Am. Midland Natural., 18:1005. and Young, M. D.: (1941) The taxonomy of the human malaria parasites, etc. Am. A. Adv. Sci., Publ., No. 15: 19. Coggeshall, L. T. (1938) Plasmodium lophurae, etc. Am. J. Hyg., 27:615. (1941) Infection of Anopheles quadrimaculatus with Plasmodium cynomolgi, and with P. lophurae. Am. J. Trop. Med., 21:525. Darling, S. T.: (1924) The spleen index in malaria. South Med. J., 17:590. (1926) Splenic enlargement as a measure of malaria. Ann. Clin. Med., 4:695. Dennis, E. W.: (1932) The life cycle of Babesia bigemina, etc. Univ. California Publ. Zool., 36:263. Downs, W. G., Gillette, H. P. S. and Shannon, R. C: (1943) A malaria survey of Trinidad and Tobago British West Indies.
:

J.

Earle, W.

in Puerto Rico. Am. J. Trop. Med., 10:207. (1939) The epidemiology of malaria with special reference to Puerto Rico. P. R. J. Pub. Health Trop. Med., 15:3. Fallis, A. M.: (1946) Plasmodium circum.flexum in ruffed grouse in Ontario. J. Parasit., 32:345.

Nat. Mai. Soc, 2:1. C: (1930) Malaria

HAEMOSPORIDIA
,

629

Davies, D. M. and Vickers, Marjorie A.: (1951) Life history of Leucocytozoon simondi, etc. Canad. J. Zool., 29:305. Ferrebee, J. W. and Geiman, Q. M.: (1946) Studies on malaria parasites. III. J. Infect. Dis., 78:173. Garnham, P. C. C.: (1948) Exoerythrocytic schizogony in malaria. Trop. Dis. Bull., 45:831. (1950) Blood parasites of East African vertebrates, etc. Parasitology, 40:328. Gonder, R. and Berenberg-Gossler, H.: (1908) Untersuchungen liber Malariaplasmodien der Affen. Malaria, 1:47. Hackett, L. W.: (1944) Spleen measurement in malaria. J. Nat. Mai. Soc, 3:121. Hartman, E.: (1927) Three species of bird malaria. Arch. Protist., 60:1. and West, E. (1941) Modification of Plasmodium cathemerium when transferred from canaries into ducks. Am. J. Hyg., 34:27. Hegner, R. and Wolfson, Fruma: (1938) Association of Plasmodium and Toxoplasma-like parasites in birds. Ibid., 28:435. Herman, C. M.: (1938) The relative incidence of blood protozoa in some birds from Cape Cod. Tr. Am. Micr. Soc, 57: 132. (1938a) Leucocytozoon anatis Wickware, a synonym for L. simondi Mathis and Leger. J. Parasit., 24:472. (1938b) Mosquito transmission of avian malaria parasites. Am. J. Hyg., 27:345. (1944) The blood parasites of North American birds. Bird Banding, 15:89. and Bischoff, A. L: (1949) The duration of Haemoproteus infection in California quail. California Fish. Game, 35:293. Hewitt, R. (1938) The cultivation of Plasmodium cathemerium for one asexual generation on inspissated egg and rabbit serum. Am. J. Hyg., 27:341. (1939) Splenic enlargement and infarction in canaries infected with a virulent strain of Plasmodium cathemerium. Ibid., 30:49. (1940) Haemoproteus metchnikovi, etc. Arch. Protist., 26:273. (1940a) Studies on blood Protozoa obtained from Mexican wild birds. Ibid., 26:287. (1940b) Bird malaria. Am. J. Hyg., Monogr. Ser. No. 15. Hogan, M. J.: (1951) Ocular toxoplasmosis. New York. Huff, C. G.: (1930) Plasmodium elongatum, n. sp., etc. Am. J. Hyg., 11:385. (1934) Comparative studies on susceptible and insusceptible Culex pipiens in relation to infections with Plasmodium cathemerium and P. relictum. Ibid., 19:123. (1935) Plasmodium hexamerium n. sp., etc. Ibid., 22:274. (1942) Schizogony and gametocyte development in Leucocytozoon simondi, etc. J. Infect. Dis., 71:18. (1947) Life cycle of malaria parasites. Ann. Rev. Microbiol.,
:
:

1:43.

030

PROTOZOOLOGY
(1948) Exoerythrocytic stages of malarial parasites. Trop. Med., 28:527.

Am.

J.

and Bloom, W.
and Coulston,

(1935)

blood and blood-forming

cells of birds. J. Infect. Dis.,

malarial parasite infecting all 57:315.

of

F.: (1944)

The development

Plasmodium

gallinaceum from sporozoite to erythrocytic trophozoite. Ibid., 75:231. (1946) The relation of natural and acquired immunity of various avian hosts to the cryptozoites and metacryptozoites of Plasmodium gallinaceum and P. relictum. Ibid., 78:
99.

(1948)

Symposium on exoerythrocytic forms

34:264.
:

of

ma-

larial parasites. II. J. Parasit.,

and Cantrell, W.
Science, 97:286. Jacobs, L. and Jones, F. E.: (1950)

(1943)

Malarial cryptozoites.

The parasitemia in experimental 87:78. James, S. P. and Tate, P.: (1938) Exoerythrocytic schizogony in Plasmodium gallinaceum. Parasitology, 30: 128. Jeffery, G. M.: (1944) Investigations on the mosquito transmission of Plasmodium lophurae Coggeshall. Am. J. Hyg., 40:251. Kikuth, W. (1931) Immunobiologische und chemotherapeutische Studien an verschiedenen Stammen von Vogelmalaria. Zentralbl. Bakt. Abt. I. Orig., 121:401. King, W. V.: (1916) Experiments on the development of malaria parasites in three American species of Anopheles. J. Exper. Med., 23:703. Kitchen, S. F.: (1938) The infection of reticulocytes by Plasmodium vivax. Am. J. Trop. Med., 18:347. (1939) The infection of mature and immature erythrocytes by P. falciparum and P. malariae. Ibid., 19:47. and Putnam, P.: (1943) Morphological studies of Plasmodium falciparum gametocytes of different strains in naturally induced infections. Ibid., 23:163. (1946) Observations on the character of the paroxysm in vivax malaria. J. Nat. Mai. Soc, 5:57. Komp, W. H. W. (1948) The anopheline vectors of malaria of the world. Proc. 4th Intern. Congr. Trop. Med. Malaria, p. 644. Kruse, W.: (1890) Ueber Blutparasiten. Virchow's Arch., 121:359. Laird, M.: (1951) Plasmodium lygosomae, etc. J. Parasit., 37:183. Laveran, A.: (1899) Les hematozoaires endoglobulaires. Cinq. soc.
toxoplasmosis.
J. Infect. Dis.,
: :

biol. jub., p. 124.

and Lucet: (1905) Deux hematozoaires de la perdrix et du dindon. C. R. Acad. Sc, 191:673. Lewert, R. M.: (1952) Nucleic acids in plasmodia and the phosphorus partition of cells infected with Plasmodium gallinaceum. J. Infect. Dis., 91:125. MacDougall, Mary S.: (1947) Cytological studies of Plasmodium: the male gamete. J. Nat. Mai. Soc, 6:91. Maegraith, B.: (1948) Pathological process in malaria and black water fever. Springfield, Illinois.

HAEMOSPORIDIA
Mantz,

631

F. A. Jr., Sailey, H. R. and Grocott, R. G.: (1949) Toxoplasmosis in Panama: report of two additional cases. Am. J. Trop. Med., 29:895. Manwell, R. D.: (1929) Relapse in bird malaria. Am. J. Hyg., 9:
308. (1934) 532. (1935)

The duration

of malarial infection in birds. Ibid., 19: Ibid.,

Plasmodium vaughani (Novy and MacNeal).

21:180. (1935a) How many species of avian malaria parasites are there? Am. J. Trop. Med., 15:265. (1939) Toxoplasma or exoerythrocytic schizogony in malaria? Riv. Malariol., 18:76. (1940) Life-cycle of Plasmodium relictum var. matutinum. Am. J. Trop. Med., 20:859. (1941) Avian toxoplasmosis with invasion of the erythrocytes. J. Parasit., 27:245. (1949) Plasmodium oli and P. hexamerium. Ibid., 35:561. and Herman, C: (1935) The occurrence of the avian malarias in nature. Am. J. Trop. Med., 15:661. Maurer, G.: (1922) Die Malaria perniciosa. Centralbl. Bakt. Orig., 32:695.

Mayer, M.:
3:3579.

(1907) Ueber Malaria beim Affen.

Med.

Klin. Berlin.,

(1908) Ueber Malariaparasiten bei Affen. Arch. Protist., 12: 314. Mayne, B. and Young, M. D.: (1941) The technic of induced malaria as used in the South Carolina State hospital. Ven. Dis. Inform., 22:271. Mercado, Teresa I. and Coatney, G. R.: (1951) The course of the blood-induced Plasmodium berghei infection in white mice. J.
Parasit., 37:479.

Milam, D. F. and Coggeshall, L. T.: (1938) Duration of Plasmodium knowlesi infections in man. Am. J. Trop. Med., 18:331. Mudrow, Lilly and Reichenow, E.: (1944) Endothelial und erythrocytare Entwicklung von Plasmodium praecox. Arch.
Protist., 97:101.

Mulligan, H. W.: (1935) Description of two species of monkey Plasmodium isolated from Silenus irus. Ibid., 84:285. Nicolle, C. and Manceaux, L.: (1909) Sur un protozoaire nouveau du Gondi (Toxoplasma n. gen.). Arch. Inst. Pasteur,
Tunis, 4:97.

Noller, W.: (1920) Die neueren Ergebnisse der Haemoproteus-

Novy,

Zuchtung. Ibid., 41:149. F. G. and MacNeal, W. J.: (1904) Trypanosomes and bird malaria. Amer. Med., Sec. I, 8:932. O'Roke, E. C.: (1934) A malaria-like disease of ducks caused by Leucocytozoon anatis Wickware. Univ. Michigan Sch. Forest. Cons. Bull., No. 4. Patton, W. H.: (1895) The name of the Southern or splenic fever
parasite.

Am.

Nat,, 29:498.

632

PROTOZOOLOGY

J. H. and Bellerive, A.: (1947) A malaria reconnaissance of the Republic of Haiti. J. Nat. Mai. Soc, 6:41. Pelaez, D., Reyes, R. P. and Barrera, A.: (1948) Estudios sobre hematozoarios. I. An. Esc. Nac. Cienc. Biol., 5:197. Porter, R. J.: (1942) The tissue distribution of exoerythrocytic schizonts in sporozoite-induced infections with Plasmodium cathemerium. J. Infect. Dis., 71:1. and Huff, C. G. (1940) Review of the literature on exoerythrocytic schizogony in certain malarial parasites and its relation to the schizogonic cycle in Plasmodium elongatum. Am. J. Trop. Med., 20:869. Raffaele, G.: (1934) Un ceppo italiano di Plasmodium elongatum. Riv. Malariol., 13:332. (1934a) Sul comportamento degli sporozoiti nel sangue del-

Paul,

l'ospite. Ibid., 13:395,706. Ratcliffe, H. L.: (1927) The relation of Plasmodium vivax and P. praecox to the red blood cells of their respective hosts as determined by sections of blood cells. Am. J. Trop. Med., 7:383. (1928) The relation of P. falciparum to the human red blood cell as determined by sections. Ibid., 8:559. Rees, C. W.: (1934) Characteristics of the piroplasms: Babesia argentina and B. bigemina in the United States. Jour. Agr. Res.,

48:427.

Regendanz,

P.

and Reichenow, E.: (1933) Die Entwicklung von

Ueber
die

Babesia canis in Dermacenter reticulatus. Arch. Protist., 79:50.

Reichenow,

E.: (1937)

Entwicklung von Theileria parva,

Bakt. Orig., 140:223. Rimington, C. and Fulton, J. D.: (1947) The pigment of the malarial parasites, P. knowlesi and P. gallinaceum. Biochem. J., 41
etc. Zentralbl.

619.

Ross, R.: (1928) Studies on malaria. London. Russell, P. F.: (1934) Malaria and Culicidae in the Philippine Islands: History and critical bibliography, 1893-1933. Dep. Agr. Comm, P.I., Tech. Bull., No. 1. (1935) The small spleen in malaria survey. Am. J. Trop. Med., 15:11. (1935a) Epidemiology of malaria in the Philippines. Am.
Ass., 26:1. (1943) Malaria and its influence on world health. Bull. New York Acad. Med., 19:599. (1952) The present status of malaria in the world. Am. J. Trop. Med. Hyg., 1:111. (1952a) Malaria: basic principles briefly stated. Springfield,
Illinois.

P.

H.

and Jacob, V. P.: (1942) On the epidemiology of malaria in the Nilgiris district, Madras Presidency. J. Med. Inst. India, 4:
349.

and Mohan, B. N.: (1942) Some mosquito hosts to avian Plasmodia with special reference to P. gallinaceum. J. Parasit.,
28:127.

HAEMOSPORIDIA
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West, L. S. and Manwell, R. D.: (1946) Practical malariology. Philadelphia. recently recognized disease Sabin, A. B.: (1942) Toxoplasmosis. of human beings. In De Sanctis: Advances in pediatrics. Schaudinn, F.: (1902) Studien iiber krankheitserregende Protozoen. II. Plasmodium vivax Grassi. Arb. kaiserl. Gesundh., 19:169. Schuffner, W. (1899) Beitrag zur Kenntnis der Malaria. Deutsche

Arch. klin. Med., 64:428. Schwarz, G. A., Rose, Eliz. K. and Fry, W. E.: (1948) Toxoplasmic encephalomyelitis, a clinical report of six cases. Pediatrics, 1:478. Sergent, Ed.: (1949) Sur deux cycles evolutifs insexues des Plasmodium chez les paludeens. C. R. Acad. Sc, Paris, 229:455.

Sergent, Ed. and Et., and Catanel, A.: (1928) Sur un parasite nouveau du paludisme des oiseaux. Ibid., 186:809. Sergent, Et. and Ed.: (1922) Etude experimentale du paludisme des oiseaux. Arch. Inst. Pasteur Afr. Nord, 2:320. Shortt, H. E. and Garnham, P. C. C.: (1948) The pre-erythrocytic development of P. cynomolgi and P. vivax. Tr. Roy. Soc. Trop.
et al.\ (1939) Malaria in Panama. Hyg., Monogr. Ser. No. 13. Sinton, J. A. and Mulligan, H. W.: (1932) A critical review of the literature relating to the identification of the malarial parasites recorded from monkeys of the families Cercopithecidae and Colobidae. Rec. Mai. Surv. India, 3:357. Smith, T. and Kilborne, F. L.: (1893) Investigations into the nature, causation and prevention of Texas or Southern cattle fever. U.S.D.Agr., Bur. An. Ind. Bull., No. 1. Starcovici, C.: (1893) Bemerkungen iiber den durch Babes entdeckten Blutparasiten, etc. Centralbl. Bakt. I. Orig., 14:1. Stratman-Thomas, W. K.: (1940) The influence of temperature on Plasmodium vivax. Am. J. Trop. Med., 20:703.

Simmons,

Med. Hyg., 41:785.' J. S., Callender, G. R.

J.

Am.

Taliaferro, W. H. and Kluver, Cessa: (1940) The hematology malaria (P. brasilianum) in Panamanian monkeys. 1, 2.
Infect. Dis., 67:121.

of
J.

and Mulligan, H. W.: (1937) The histopathology of mawith special reference to the function and origin of the macrophages in defence. Indian Med. Res., Memoires, 29:1. Taliaferro, W. H. and Lucy, G.: (1934) Morphology, periodicity and course of infection of P. brasilianum in Panamania monlaria

keys.

Hyg., 20:1. (1947) Asexual reproduction of P. cynomolgi in rhesus monkeys. J. Infect. Dis., 80:78. (1949) Asexual reproduction of P. knowlesi in rhesus
J.

Am.

monkeys. Ibid., 85:107. Terzian, L. A.: (1941) Studies on P. lophurae, a malarial parasite
in fowls.
I.

Am.

J.

Hyg., 33:

1.

Thompson,
site,

and Huff, C. G.: (1944) A saurian malarial paraP. mexicanum, n. sp., etc. J. Infect. Dis., 74:48,
P. E.

634

PROTOZOOLOGY

(1944a) Saurian malarial parasites of the United States and Mexico. Ibid., 74:68. Thomson, J. G.: (1928) Stippling of the red cells in malaria. Proc. Roy. Soc. Med., 21:464. Toit, P. J. D.: (1918) Zur Systematik der Piroplasmen. Arch. Protist., 39:84. Trager, W. (1950) Studies on the extracellular cultivation of an intracellular parasite (avian malaria). I. J. Exper. Med., 92: 349. Vincke, I. H. and Lips, M.: (1948) Un nouveau Plasmodium d'un rougeur sauvage du Congo, P. berghei, n. sp. Ann. Soc. Beige med. trop., 28:97. Wampler, F. J.: (1930) A preliminary report on the early effects of plasmochin on P. cathemerium. Arch. Protist., 69: 1. Warren, A. J. and Coggeshall, L. T.: (1937) Infectivity of blood and organs in canaries after inoculation with sporozoites. Am. J.
:

Hyg.,26:l

Weinman,
more.

D.: (1952) Toxoplasma and toxoplasmosis. Ann. Rev. Microbiol., 6:281. Wenyon, C. M.: (1926) Protozoology. Vol. 2. London and Balti-

A. B.: (1915) Is Leucocytozoon anatis the cause of a new disease in ducks? Parasitology, 8:17. Wolfson, Fruma: (1936) Plasmodium oti n. sp., etc. Am. J. Hyg.,
24:94. (1940) Virulence and exoerythrocytic schizogony in four species of Plasmodium in domestic ducks. J. Parasit., 26:Suppl.:
28.

Wickware,

(1941) Avian hosts for malaria research. Quart. Rev. Biol., 16:462. and Winter, Mary W. (1946) Studies of P. cynomolgi in the rhesus monkey, Macaca mulatto.. Am. J. Hyg., 44:273. Wood, S. F. and Herman, C. M.: (1943) The occurrence of blood parasites in birds from southwestern United States. J. Parasit., 29:187. Yorke, W. and MacFie, J. W. S.: (1924) Observations on malaria made during treatment of general paresis. Tr. Rov. Soc. Trop. Med. Hyg., 18:13.
:

Chapter 27
Subclass 2 Acnidosporidia Cepede
sporozoa which THE known, although some
are grouped here are mostly incompletely

of them are widely distributed. They produce spores which are simple in structure, being composed of a spore membrane and a sporoplasm.

Order

Haplosporidia Caullery and Mesnil

spores. In

This order includes those sporozoans which produce simple some species the spores may resemble superficially those of Microsporidia, but do not possess any polar filament. In this regard, Haplosporidia may be considered a more primitive group than

Cnidosporidia (p. 643). The Haplosporidia are cytozoic, histozoic, or coelozoic parasites of invertebrates and lower vertebrates. The spore is spherical or
ellipsoidal in

form and covered by a resistant membrane which may

possess ridges or

may

be prolonged into a more or

less

long tail-like

projection. In a few species the spore

membrane

possesses a lid

when opened, will enable the sporoplasm to emerge as an amoebula. The sporoplasm is uninucleate and fills the intrasporal
which,
cavity.

The development
teum, as worked out

of a haplosporidian,

Ichthyosporidium gigan-

by Swarczewsky,

is

as follows (Fig. 271):

The

spores germinate in the alimentary canal of the host fish and the emerged amoebulae make their way to the connective tissue of vari-

ous organs (a). These amoebulae grow and their nuclei multiply in number, thus forming plasmodia. The plasmodia divide into smaller bodies, while the nuclei continue to divide (b-e). Presently the nuclei become paired (/, g) and the nuclear membranes disappear (Ji). The

plasmodia now break up into numerous small bodies, each of which contains one set of the paired nuclei (i, j). This is the sporont (j) which develops into 2 spores by further differentiation (k-o). Genus Haplosporidium Caullery and Mesnil. After growing into a large form, Plasmodium divides into uninucleate bodies, each of which develops into a spore; spore truncate with a lid at one end;
envelope sometimes prolonged into processes; in aquatic annelids

and molluscs. H. chitonis (Lankester)

(Fig. 272, a, b).

tissue of Craspidochilus cinereus; spores oval, 10m

In liver and connective by 6m; envelope

with 2 prolonged projections.

635

036

PROTOZOOLOGY
(Fig. 272, c).

H. limnodrili Granata

In gut epithelium of Lim8-10/x.

d).

nodrilus udekemianus; spores 10-12m

by

H. nemertis Debaisieux (Fig. 272, Lineus bilineatus; spores oval with a

flat

In connective tissue of operculum, but without

any projections of envelope, 7m by 4m. H. heterocirri C. and M. (Fig. 272,

e).

In gut epithelium of Het-

Fig. 271. The development of Ichthyosporidium giganteum (Swarczewsky). a-e, schizogony; f-n, sporogony; o, stained spore, X about 1280.

erocirrus viridis;

mature organisms 50-60m by 30-40/x; spores 6.5m

by

4m.

H. scolopli C. and M. (Fig. 272, /). In Scoloplos mulleri; fully grown form 100-150m by 20-30m; spores 10m by 6.5m. H. vejdovskii C. and M. (Fig. 272, g). In a freshwater oligochaete,
Mesenchytraeus flavus ; spores 10-12m long. Genus Urosporidium Caullery and Mesnil. Similar to Haplosporidium, but spherical spore with a long projection.

ACNIDOSPORIDIA, HAPLOSPORIDIA
U. fuliginosum C. and

637

M.

(Fig. 272, h,

i).

In the coelom of the

to

polychaete, Syllis gracilis; rare.

Genus Anurosporidium Caullery and Chappellier. Similar

H aplosporidium, but operculate spore spherical.

Donax trunculus; schizogony intracellular; up to 200 spores; spores about 5m long.
A. pelseneeri C. and C. In sporocyst of a trematode parasitic in cysts extracellular, with

a, b, H aplosporidium chitonis, X1000 (Pixell-Goodrich;) c, H. X1000 (Granata); d, H. nemertis, X1000 (Debaisieux); e, H. heterocirii, X 1000 (Caullery and Mesnil) f H. scolopli, X 1000 (Caullery and Mesnil); g, H. vejdovskii, X1000 (Caullery and Mesnil); h, i, Urosporidium fuliginosum. X1000 (Caullery and Mesnil); j, k, Bertramia asperospora (j, cyst with spores; k, empty cyst), X1040 (Minchin); 1, m, Coelosporidium periplanetae (1, trophozoite with spores and chromatoid bodies), X2540 (Sprague).

Fig. 272.

lirnnodrili,

Genus Bertramia Caullery and Mesnil. Parasitic in aquatic worms and rotifers; sausage-shaped bodies in coelom of host; spherical spores which develop in them, possess a uninucleate sporoplasm and a well-developed membrane. B. asperospora (Fritsch) (Fig. 272, j, k). In body cavity of rotifers: Brachionus, Asplanchna, Synchaeta, Hydatina, etc.; fully grown vermicular body 70-90m with 80-150 spores.

G3S

PROTOZOOLOGY
M.
In the annelid Capitella capitata; spores
diameter.

B. capitellae C. and
2.5/x in

B. euchlanis Konsuloff. In coelom of rotifers belonging to the

genus Euchlanis. Genus Ichthyosporidium Caullery and Mesnil. In fish; often looked upon as Microsporidia, as the organism develops into large bodies in body muscles, connective tissue, or gills, which appear as
conspicuous "cysts," that are surrounded by a thick wall and contain
/.

numerous

spores.

giganteum (Thelohan) (Fig. 271). In various organs of Crenilabrus melops and C. ocellatus; cysts 30m-2 mm. in diameter; spores
5-8/i long.
I.

hertwigi Swarczewsky. In Crenilabrus paro; cysts 3-4

mm.

in

diameter in gills; spores 6m long. Genus Coelosporidium Mesnil and Marchoux. In coelom of Cladocera or Malpighian tubules of cockroach; body small, forming cysts; spores resemble microsporidian spores; but without a polar
filament.
C. periplanetae (Lutz

and Splendore)

(C. blattellae

Crawley)

(Fig.

m). In lumen of Malpighian tubules of cockroaches; spores 5.5-7. 5/x by 3-4^. Cytology (Sprague, 1940).
272,
1,

common;

Order 2 Sarcosporidia Balbiani

These organisms are muscle parasites

tiles.

of

The

infected host muscles are characterized

mammals, birds and repby the presence of

which vary from

opaque white bodies (Miescher's

tubes) (Fig. 273)

microscopic to several centimeters in length, and are cylindrical, ellipsoid or ovoid, with a somewhat lobulated surface. When mature, the parasite becomes- filled with the "spores" or Rainey's corpuscles

which are crescentic or banana-shaped. They contain a nucleus and many granules, surrounded by a very delicate membrane (Fig. 274). The morphological peculiarity and lack of information concerning their transmission and development have characterized these organ-

Fig. 273.

a,

ana

in the

Sarcocystis tenella in the oesophagus of sheep; b, S. miescherimuscle of pig; XI (Schneidemuhl from Doflein).

ACNIDOSPORIDIA, SARCOSPORIDIA
isms for
sterile

639

many years.

Spindler and

Zimmerman

(1945) placed asepti-

cally ruptured cysts of Sarcocystis miescheriana (p. 640) of pigs in

dextrose solution and kept the preparations at 37C. for 24 hours and then at room temperature. In from a few days to two weeks, the "spores" budded off minute, coccoid bodies which developed into septate mycelia with vertical hyphae bearing spores, a typical feature of the development of a fungus belonging to Aspergillus. When the conidia from the cultures were injected into or fed
to 50

young

pigs,

25 showed at necropsy four to

six

months

after the

injection or ingestion of the conidia, typical Sarcocystis cysts in the

muscles, while the controls remained free from infection. Cultures

made from

the mature cysts in these pigs, developed a fungus like

that which had been injected. Pigs, rats and mice which fed on the
cysts, passed faeces and urine containing yeast-like bodies which developed in cultures into a fungus like that which was originally cultured. Spindler 's (1947) further study revealed that in the sarco-

sporidian cysts of sheep and duck, the strands present within the

and the compartments contained a network of jointed hypha-like structures, and the spores appeared to be exogenous growths on the jointed hypha-like structures; and each spore was capable of budding out another spore from its free end. Spindler concludes from these observations that Sarcocystis of pigs, sheep and ducks are fungi, related to Aspergillus. This view will explain reasonably well the difficulties
encountered in relation to Sarcosporidia; namely, the unknown life cycle, lack of a protective membrane of the "spore," the absence of a vector, and the common occurrence among herbivorous animals. Genus Sarcocystis Lankester. In the muscles of higher vertebrates. Many species have been reported by various workers from mammals, birds and reptiles on the basis of difference in host species. Species
(Babudieri, 1932).
S. lindemanni (Rivolta). A few cases of Sarcocystis infection have been reported from man in muscle cells of larynx (Baraban and St. Remy), of biceps and tongue (Darling), of heart (Manifold), of breast (Vasudevan), etc. There seem to be dimensional discrepancies of organisms observed by different investigators. The dimensions of parasitic masses and of spores are as follows Parasites 1.6 mm. by 170m and banana-shaped spores 8-9/z long (Baraban and St. Remy) parasites 84ju by 27m and spores 4.25m by 1.75m (Darling) parasites spherical, 500/* in diameter and spores over 10m long (Manifold); parasites 5.3 cm. by 320m and spores 8.33m by 1.6m (Vasudevan). The parasitic masses are oval to spindle in form and
:

cysts were none other than the connective tissues of the host

640

PROTOZOOLOGY
in the

imbedded

muscle

cells

which are distended, and

may
is

appear
divided

white-streaked to naked eye. Seen in sections, the body

into compartments. Gilmore,

Kean and Posey (1942) have recently found three bodies in sectioned heart muscles of an eleven year old child who died from an unknown cause, and considered them as sarcosporidian bodies. They measured 25m by 19m, 57m by 30m, and 41m by 25m hi cross sections; there were no septa within the bodies; minute bodies present in the masses were mostly rounded and about 1m in diameter, though a few were crescentic. The questions such as what species infect man, how man becomes infected, etc., are unanswered at present.
Muscle layer
Connective tissue layer
Fibrous zone
External}

Median /Cyst membrane

Internal

Sporoblasts

Spores

Fig. 274. Portion of a cyst of Sarcocystis tenella in sheep,

about

1000 (Alexeieff).
S. tenella Railleit (Figs. 273, a; 274). In the muscles of tongue,

pharynx, oesophagus, larynx, neck, heart, etc., of sheep; large parasites 40m~2 cm. long with a thin membrane; spores sickleform
(Alexeieff, 1913; Scott, 1943).

S. miescheriana (Kiihn) (Fig. 273, b). In the muscles of pig; cysts

up to 3-4 mm. by 3 mm.; envelope

striated; "spores" reniform.

Musfeldt (1950) found 15 of 264 pig diaphragms examined were infected by a Sarcocystis. The pigs were all garbage-fed animals.

ACNIDOSPORIDIA, SARCOSPORIDIA

641

Sarcocystis infections were also noticed in the rats from one of the
piggeries

the organism

from which infected pigs were obtained. Fungus nature of (p. 639); effect on host (Spindler, Zimmerman and

Jaquette, 1946).
S. bertrami Doflein. In the muscles of horse; similar to S. miescheriana; parasitic mass up to 9-10 mm.; envelope striated. S. muris Blanchard. In body muscles of rats and mice; parasitic masses up to 3 cm. long; spores 13-15/x by 2.5-3/*; transmissible to guinea pig (Negri) which shows experimental infection in muscles in 50-100 days after feeding on infected muscles. S. rileyi Stiles. In muscles of various species of ducks; parasites in muscle, opaque white in color and measure up to 5 mm. by 2 mm.; spores are sausage-shaped and 8-10/i by about 3;u.

References

Alexeieff, A.: (1913) Recherches sur Sarcosporidies.

I.

Arch. zool.

exper. gen., 51:521. Babudieri, B.: (1932) I Sarcosporidi e le Sarcosporidiose. Arch.

Protist., 78:421.

Baraban,

L. and St. Remy, G.: (1894) Sur une cas de tubes psorospermiques observes chez l'homme. C. R. soc. biol., 10:201. Caullery, M. and Mesnil, F.: (1905) Recherches sur les Haplosporidies. Arch. zool. exper. gen., 4:101. Crawley, H.: (1914) The evolution of Sarcocystis muris in the intestinal cells of the mouse. Proc. Acad. Nat. Sc. Philadelphia,

66:432.

Darling, S. T.: (1909) Sarcosporidiosis, with report of a case in man. Arch. Int. Med., 3:183 (1919) Sarcosporidiosis in an East Indian. J. Parasit., 6:98. Gilmore, H. R. Jr., Kean, B. H. and Posey, F. M.: (1942) A case of sarcosporidiosis with parasites found in heart. Am. J. Trop.
Med., 22:121.

Lambert, S. W.: (1927) Sarcosporidial infection of the myocardium in man. Am. J. Path., 3:663. Musfeldt, I. W. (1950) A report on infection by Sarcocystis sp. in swine from Vancouver, Canada. Canad. J. Comp. Med. Vet.
:

Sc, 14:126. Scott, J. W.: (1943) Life history of Sarcosporidia, with particular reference to Sarcocystis tenella. Bull. Univ. Wyoming Exper.
Stat., no. 259.

Spindler, L. A.: (1947)

A note on the fungoid nature of certain internal structures of Miescher's sacs, etc. Proc. Helm. Soc. Washington, 14:28. and Zimmerman, H. E. Jr.: (1945) The biological status of Sarcocystis. J. Parasit., 31 :suppl. 13. and Jaquette, D. S.: (1946) Transmission of Sarcocystis to swine. Proc. Helm. Soc. Wash., 13: 1.

642

PROTOZOOLOGY

Sprague, V.: (1940) Observations on Coelosporidium periplanetae with special reference to the development of the spore. Tr. Am. Micr. Soc, 59:460. Swaczewsky, B.: (1914) Ueber den Lebenscyklus einiger Haplo-

Teichmann,

Handbuch der pathog. Protozoen. Part 3:345. Weissenberg, R.: (1921) Fischhaplosporidien. Ibid., Part 3:1391.

sporidien. Arch. Protist., 33:49. E.: (1912) Sarcosporidia. Prowazek's

Chapter 28
Subclass 3 Cnidosporidia Doflein
subclass possess without exception members THE unique Each spore ant spores which are
of this
of
resist-

structure.

possesses

1-4 polar filaments and one to manjr sporoplasms. The membrane which envelops these structures may be a single-piece or bi- or trivalved.

The

polar filament

is

typically coiled within a polar capsule.

In the order Myxosporidia and Actinomyxidia, there appear several cells during the process of sporulation. These cells give rise
to one
cells,

to

many

sporoplasms or generative

cells,

capsulogenous

and spore membrane. This condition is not observed in other groups of Protozoa and for this reason some writers recognize a close affinity between these two orders and the Mesozoa. The method of multiplication in the Cnidosporidia is schizogonic and sporogonic.

The

division

is

repeated binary or multiple

fission,

budding, or

plasmotomy. The nuclear division varies from amitosis to mitosis. Isogamous, anisogamous, and autogamous reproduction have been
reported in a

number

of species. In

many

forms, the zygote

differentiated.

is

the

sporont, in which one to

many

spores

become

secondary or intermediate host has been found for any of the They are exclusively parasites of the lower vertebrates and invertebrates. Since cnidosporidian infections occur frequently in epidemic forms among such economically important animals as the silkworm, honey bees, and commercial fishes, these organisms possess considerable practical significance. History and
Cnidosporidia.

No

economic importance (Auerbach, 1910; Kudo, 1920, 1924). The Cnidosporidia are divided into the following four orders:
Spores comparatively large Shell bivalve; 1 to 4 polar capsules Shell trivalve; 3 polar capsules Spores comparatively small
Shell one-piece;

Order 1 Myxosporidia Order 2 Actinomyxidia (p. 660)

1 (or 2) polar filament. .Order 3 Microsporidia (p. 668) Barrel-shaped; a thick filament coiled beneath the shell; 3 sporoplasms Order 4 Helicosporidia (p. 678)

Order

Myxosporidia Butschli
is

The

spore of a myxosporidian

of various shapes

and dimen-

sions. It is

covered by a bivalve chitinous spore membrane (Kudo, 1921), the two valves meeting in a sutural plane which is either twisted (in three genera) or more or less straight. The membrane may possess various markings or processes. The polar capsule, with
643

644
its

PROTOZOOLOGY
short coiled filament, varies in

number from one

to four (Fig.

275).
is

Except

in the family Myxidiidae, in

which one polar capsule

situated near each of the poles of the spore, the polar capsules
is

are always grouped at one end which

ordinarily designated as the

anterior end of the spore.

polar capsules, there

is

between (in Myxidiidae) the almost always a sporoplasm. Ordinarily a

or

Below

Fig. 275. Sporogony in Myxosoma catostomi, X2130 (Kudo), a, sporont or pansporoblast; b-h, development of two sporoblasts within the sporont; i, a nearly mature spore; j-1, views of spore.

young spore possesses two sporoplasm nuclei which fuse into one (autogamy) when the spore becomes mature. In Myxobolidae there is a glycogenous substance in a vacuole which stains mahogany red with iodine and is known as the iodinophilous (iodophile) vacuole.

The Myxosporidia

are

brates, especially fishes.

Both

exclusive^ parasites of lower vertefresh and salt water fishes have been

found to harbor, or to be infected by, Myxosporidia in various regions of the world. A few occur in Amphibia and Reptilia, but no species has been found to occur in either birds or mammals. When a spore gains entrance into the digestive tract of a specific host fish, the sporoplasm leaves the spore as an amoebula which penetrates through the gut-epithelium and, after a period of migration, enters the tissues of certain organs, where it grows into a trophozoite at the

CNIDOSPORIDIA, MYXOSPORIDIA

645

expense of the host tissue cells, and the nucleus divides repeatedly. Some nuclei become surrounded by masses of dense cytoplasm and become the sporonts (Fig. 275). The sporonts grow and their nuclei divide several times, forming 6-18 daughter nuclei, each with
a small mass of cytoplasm. The number of the nuclei thus produced depends upon the structure of the mature spore, and also upon whether 1 or 2 spores develop in a sporont. When the sporont develops into a single spore, it is called a monosporoblastic sporont, and if two spores are formed within a sporont, which is usually the
case, the sporont is called disporoblastic, or pansporoblast.

The

spore-formation begins usually in the central area of the large trophozoite, which continues to grow.

The surrounding host

tissue

becomes degenerated or modified and forms an envelope that is often large enough to be visible to the naked eye (Figs. 278, 280). This is ordinarily referred to as a myxosporidian cyst. If the site of infection is near the body surface, the large cyst breaks and the mature spores become set free in the water. In case the infection is confined to internal organs, the spores will not be set free while the host
fish lives.

Upon

its

death and disintegration of the body, however,

the liberated spores

become the source

of

new

infection.

The more

primitive Myxosporidia are coelozoic in the host's

organs, such as the gall bladder, uriniferous tubules of the kidney,

urinary bladder,
their

etc.

way

into the specific organ

In these forms, the liberated amoebulae make and there grow into multinucleate

of various types.

amoeboid trophozoites which are capable of forming pseudopodia They multiply by exogenous or endogenous budding or plasmotomy. One to several spores are developed in the
trophozoite.

Almost

all

observers agree in maintaining the view that the 2

nuclei of the sporoplasm or 2 uninucleate sporoplasms fuse into one

(autogamy or paedogamy), but as to the nuclear as well as cytoto, and during, spore-formation, there is a diversity of opinions. For illustration, the development of Sphaeromyxa sabrazesi (p. 656) as studied by two investigators may be taken as an example. Debaisieux's (1924) observation is in brief as follows (Fig. 276) Sporoplasms after finding their way into the gall bladder
plasmic changes prior
:

of host fish develop into large trophozoites containing

(a, 6)

many

nuclei

2 vegetative nuclei become surrounded

by a cytoplasmic mass(c)

and this develops into a primary propagative cell (d) which divides (3 chromosomes are noted) (e) and forms secondary propagative cells (/). A binucleate sporocyte is formed from the latter by unequal nuclear division (g-j) and 2 sporocytes unite to form a tetranucleate

646

PROTOZOOLOGY
(j)

which develops into 2 spores (k, I). Sporoplasm (/), but later 4 (ra>), of which 2 degenerate (n) and the other 2 fuse into one nucleus (o). On the other hand, according to Naville(1930) a uninucleate amoebula (Fig. 277, a) enters the gall bladder and develops into multinucleate trophozoite in which nuclear
pansporoblast

shows

first

2 nuclei

b
c

The development of Sphaeromyxa sabrazesi (Debaisieux). vegetative nuclei; b, association of two vegetative nuclei; c, the same within a cell; d, primary propagative cell; e, its division; f, secondary propagative cells; g, their division; h, formation of sporocyte; i, two sporocytes; j, formation of pansporoblast; k, pansporoblast at later stages; 1, pansporoblast with two spores, the sporoplasm of which contains two nuclei; m, four nuclei in sporoplasm; n, two nuclei remain functional, the other two degenerate, o, fusion of the two nuclei.
Fig. 276.
a,

CNIDOSPORIDIA, MYXOSPORIDIA

647

Fig. 277. The development of Sphaeromyxa sabrazesi (Naville). a, uninucleate amoebula enters the gall bladder; b, young multinucleate trophozoite; c, development of macrogametes; d, development of microgametes; e, f, plasmogamy; g-m, development of pansporoblast; n, fusion of the two nuclei in the sporoplasm.

648

PROTOZOOLOGY

division reveals 4 chromosomes (6); within the trophozoite macrogametes and microgametes are independently formed, during which process, chromosome number is reduced into half (2) (c, d) plasogamy between a macrogamete and a microgamete results in production of a binucleate pansporoblast (e,f), from which repeated nuclear division (g-l) forms 2 spores (m) each of the 2 nuclei of the sporoplasm is haploid and the diploid number is restored when the 2 nuclei fuse into one (n). The site of infection by Myxosporidia varies among different species. They have been found in almost all kinds of tissues and organs of host fish, although each myxosporidian has its special site of infection in one to several species of fish. The gills and gall bladder are most frequently parasitized by Myxosporidia in freshwater fishes, while the gall bladder and urinary bladder of marine fishes harbor one or more species of Myxosporidia. When the infection is concentrated in the fins or integument, the resulting changes are
;

quite conspicuous (Fig. 278).

The

infection in the gills

is

usually

Fig. 278.

channel cat, heavily infected with Henneguya X* (Kudo).

exilis,

manifest by whitish pustules which can be frequently detected with the unaided eye. When the wall of the alimentary canal, mesentery, liver, and other organs are attacked, one sees considerable changes in them. Heavy myxosporidian infection of the gall bladder or uri-

nary bladder of the host fish may cause abnormal appearance and coloration or unusual enlargement of the organ, but under ordinary circumstances the infection is detected only by a microscopical examination of its contents. Certain histological changes in the host

have been mentioned elsewhere (p. 31). Severe epidemic diseases of fishes are frequently found to be due to myxosporidian infections. According to Davis (1924), the "wormy" halibut of the Pacific coast of North America is due to the myxofish

sporidian, Unicapsula muscalaris (Fig. 280), which invades the

mus-

cular tissue of the host

fish.

The

"boil disease" of the barbel, Barbus

is

barbus and others, of European waters,

pfeifferi (Keysselitz, 1908).

Myxosoma

cerebralis,

caused by Myxobolus which attacks the

CNIDOSPORIDIA, MYXOSPORIDIA
supporting tissues of salmonid
cially to
fish, is

649

known

so-called "twist disease" (Plehn, 1904),

and occurs in body muscles of various species of Pacific salmon and produces opaque white cysts, 3-6 mm in diameter; it is thus responsible for the so-called "tapioca disease" of salmon (Fish, 1939). Kudoa thyrsites (p. 655) attacks the body muscle fibers of the barracouta in which the infected muscles become liquefied. This condition is known as "milky barracouta" or "pap snoek" and may
fishes

young

to be responsible for the which is often fatal espean epidemic form. Henneguya

salminicola invades the

affect as

much as 5 per cent of the commercial catches (Willis, 1949). Taxonomy (Gurley, 1894; Thelohan, 1895; Auerbach, 1910; Kudo,
1920, 1933); development (Kudo, 1920; Naville, 1927, 1930; Noble,

1944); species from North America (Gurley, 1894; Mavor, 1915, 1916; Davis, 1917; Kudo, 1920-1944; Jameson, 1929, 1931; Meglitsch,

1937-1947a; Fantham et ah, 1939, 1940; Noble, 1939, 1941; Rice and Jahn, 1943), from South America (da Cunha and Fonseca, 1917, 1918; Nemeczek, 1926; Pinto, 1928; Guimaraes, 1931), from
1912; Jameson, 1913; Georgevitch, 1916-1936; Dunkerly,

Europe (Thelohan, 1895; CSpede, 1906; Auerbach, 1910, 1912;

Parisi,

1921; Petruschewsky, 1932; Jaczo, 1940); from Asia (Fujita, 1923,

1927; Chakravarty, 1939, 1943; Chakravarty and Basu, 1948).

The Myxosporidia

are divided into three suborders:

Largest diameter of spore at right angles to sutural plane; with 1 polar capsule on each side; sporoplasm without iodinophilous vascuole.
.

Eurysporea Spore spherical or subspherical with 1, 2, or 4 polar capsules; sporoplasm without iodinophilous vacuole. .Suborder 2 Sphaerosporea (p. 651) Sutural plane coincides with, or is at an acute angle to, largest diameter of spore; 1, 2, or 4 polar capsules; sporoplasm with or without iodinoSuborder 3 Platysporea (p. 655) philous vacuole
Suborder
1

Suborder

Eurysporea Kudo
fish,

Spores laterally expanded; coelozoic in marine

Spores less laterally expanded; in freshwater

except one species.

1

Family

Ceratomyxidae
(p.

fish; histozoic or coelozoic.

Family 2 Wardiidae

651)

Family

Ceratomyxidae Doflein

Spores are laterally prolonged and therefore sutural diameter is smaller than width; 2 polar capsules at anterior margin; one on

each side of sutural plane; in one genus the spores contain three polar
capsules and the spore

membrane is composed Genus Ceratomyxa Thelohan. Shell-valves

of three shell-valves.

conical

and hollow,

650

PROTOZOOLOGY

attached on bases; sporoplasm usually not filling intrasporal cavity; Numerous species in the gall-bladder of marine fish, except C. shasta
(Noble, 1950) which was found "widely distributed in viscera" of
fingerling

rainbow trout (Salmo gairdneri).

Fig. 279. a, Ceratomyxa mesospora, X1000 (Davis); b, c, C. hopkinsi, X1000 (Jameson); d-j, Leptotheca ohlmacheri (d, section of a uriniferous tubule of Rana pipiens, with trophozoites and spores, XS00; e, a trophozoite with a

polar filaments;

bud; f-h, disporous trophozoites; i, a spore with extruded X1500) (Kudo). j, surface view of spore,

CNIDOSPORIDIA, MYXOSPORIDIA
C. mesospora

651

Davis

(Fig. 279, a).

In the gall-bladder of Cestracion

zygaena; spores 8m in sutural diameter and 50-65m wide. C. hopkinsi Jameson (Fig. 279, b, c). In the gall-bladder of Parophrys vetulus, Microstomias pacificus and Citharichthys xanthostigmus
trophozoites disporous; spores 5. 7-7. 5m in sutural diameter and 28.839m broad. Genus Leptotheca Thelohan. Shell-valves hemispherical; in gallbladder or urinary bladder of marine fish and one in amphibians.

Numerous

species.

L. ohlmacheri (Gurley) (Fig. 279, d-j). In the uriniferous tubules of

kidney of frogs and toads; spores 9.5-12m in sutural diameter and 13-14. 5ju wide; with 2 uninucleate sporoplasms (Kudo 1922). Genus Myxoproteus Doflein. Spores pyramidal with or without distinct processes at base of pyramid; in urinary bladder of marine
fish.

3 species.
.

cordiformis Davis (Fig. 280, a). In the urinary bladder of Chae-

by 10-1 1mGenus Trilospora Noble. Spores triangular with concave sides in anterior end-view; profile ellipsoid; three polar causles and three shell-valves; in the gall-bladder of marine fish. One species. T. californica N. Spores 7.2/x in sutural diameter by 16/z wide; polar capsules 3/x by 1.5/i, often four instead of three in number; in the gall-bladder of Typhlogobius californiensis and Gibbonsia elegans
(odipterus faber; spores 12 m

elegans (Noble, 1939).

Family 2 Wardiidae Kudo

Genus Wardia Kudo. Spores

fish.

isosceles triangle with 2

convex

sides;

oval in profile; 2 large polar capsules; tissue parasites of freshwater

2 species.

(Fig. 280, 6). In the ovary of Lepomis humilis; spores 9-1 1m in sutural diameter and 10-12m wide. Genus Mitraspora Fujita. Spores circular or ovoidal in front view;

W. ovinocua K.

somewhat

flattened in profile; 2 polar capsules; shell striated; with

or without posterior filaments; in kidneys of freshwater

suborders. 3 species.

fishes. This genus apparently includes border-line forms between this and other

M.

elongata

Kudo. In the kidney

.

of Apomotis cyanellus; spores

15-17m by 5-6 M

Suborder 2 Sphaerosporea Kudo

Spore with 1 polar capsule Spore with 2 polar capsules Spore with 4 polar capsules

Family l Unicapsulidae Family 2 Sphaerosporidae Family 3 Chloromyxidae

652) 653) (p. 654)

(p.

(p.

652

PROTOZOOLOGY
Family
1

Unicapsulidae

Kudo
1

Genus Unicapsula Davis. Spherical spore with

fish.

polar capsule;

shell-valves asymmetrical; sutural line sinuous; histozoic in marine

One species.

X 1000 (Davis) b, Wardia ovinoSphaerospora polymorpha, X1000 (Davis); d-i, S. tincae (d, external appearance of a heavily infected young tench; e, internal appearance, Xf f, mature pansporoblast; g, h, two spores; i, germination of spore, X1000) (L6ger); j, k, Sinuolinea dimorpha (j, trophozoite with three gemmules, X420; k, a spore, X930) (Davis); 1, m, ChloroFig. 280. a, Myxoproteus cor difor mis,
;

cua,

X1330 (Kudo);

c,

myxum
(Kudo).

leydigi

(1,

X500; m, X1000) (Th&ohan);

n, C. trijugam,

X1130

U. muscularis D. (Fig. 281). Spore about 6m in diameter; 2 uni-

nucleate sporoplasms; in muscle fibers of halibut; Pacific coast of

North America; the cause of the "wormy" halibut (Davis, 1924).

CNIDOSPORIDIA, MYXOSPORIDIA
Family 2 Sphaerosporidae Davis

653

Genus Sphaerospora Thelohan. Spore

histozoic in marine or freshwater fishes.

spherical or subspherical

sutural line straight; 2 polar capsules at anterior end; coelozoic or

Fig. 281. Unicapsula muscularis (Davis),

a, b,

X20; c, cross-section of an infected muscle, X190; an infected muscle, X575; e-h, spores, X2500.

infected muscle fibers, d, part of a section of

S. polymorpha Davis (Figs. 280, c; 282, a-e). In the urinary bladder of toadfish, Opsanus tau and 0. beta. Trophozoites amoeboid with conical pseudopodia; up to 100/x long, the majority being 20-5(V

long;

plasmotomy; disporoblastic; disporous or polysporous. Spores

spheroidal; shell-valves finely striated; polar capsules divergent;

fresh spores

measure 7. 5-9. 5m by 7-8/*. quently infection by Nosema notabilis hyperparasitism (Kudo, 1944).

The
(p.

trophozoites suffer fre-

672).

Development and

654

PROTOZOOLOGY

S. tincae Plehn (S. pernicialis Leger) (Fig. 280, d-i). In the kidney and other viscera of Tinea tinea in France and Germany; cause of epidemic disease among young tench; disease is manifest by great distension of anterior portion of abdomen and up-turned mouth in:

Fig. 282. a-e, Sphaerospora polymorpha (Kudo) (a, a trophozoite in life, b, stage in simple plasmotomy, X700; c, d, front and anterior end views of fresh spores; e, a spore with the extruded polar filaments, X1415);f-h, Myxidium. serotinum (Kudo) (f, a stained young trophozoite, XI 530; g, h, two views of fresh spores, showing the ridges on the mem-

XI 530;

brane, X915); stained spores,

clupeidae (Meglitsch) (i, j, two views of unstained spores, X1430); m-p, K. thyrsites 1, (Willis) (m-o, preserved spores; p, a spore from section).
i-1,

Kudoa

X1240;

k,

fection fatal through rupture of abdominal wall; spores 7-8.75/* in

diameter (Leger, 1929). Genus Sinuolinea Davis. Spherical or subspherical spores; sutural line sinuous; with or without lateral processes; 2 spherical polar capsules; in urinary bladder of marine fish. S. dimorpha D. (Fig. 280, j, k). In Cynoscion regalis; spores 15m in diameter (Davis, 1917).

Family 3 Chloromyxidae Thelohan

Genus Chloromyxum Mingazzini. Spore with 4 polar

grouped at anterior end;
shell

capsules,

surface often striated or ridged;

CNIDOSPORIDIA, MYXOSPORIDIA
histozoic or coelozoic in freshwater or marine fish
ians.

655

and

also in

amphib-

c, d; 280, I, m). In the gall-bladder of variC. ous species of Raja, Torpedo and Cestracion; spores 6-9/x by 5-6ju; widely distributed. Structure and development (Erdmann, 1917;

Numerous species. leydigi M. (Figs. 70,

Naville, 1927).
C. trijugum

Kudo

(Fig. 280, n). In the gall-bladder of Xenotis

megalotis

and Pomoxis sparoides; spores 8-10/x by 57/x. Genus Kudoa Meglitsch. Resembles Chloromyxum; but spores
quadrate
in anterior

stellate or

end-view; spore

membrane

delicate

and the sutures

litsch, 1947a).

indistinct; four shell-valves (?); histozoic

(Meg-

Several species.
(Fig.

K. clupeidae (Hahn)

282, i-l).

In the body muscles of

spores 5.1m by 6.4m; polar capsules 1.5m by 1m (Meglitsch, 1947). Nigrelli (1946) found this species in the ocean pout {Macrozoares americanus).

Clupea harengus, Brevoortia tyrannus,

etc.;

K.

thyrsites (Gilchrist) (Fig. 282,

m-p). In the body muscles of the

barracouta, Thyrsites atun, in Australia and Africa; pyramidal spores

6-7 m high and 12-1 7 m wide; two uninucleate sporoplasms; polar capsules homogeneous in appearance (Willis, 1949). Effect on host
(p. 649).

Suborder 3 Platysporea Kudo

Without iodinophilous vacuole 2 polar capsules, one at each pole
polar capsule 2 or 4 polar capsules grouped With an iodinophilous vacuole
1

Family 1 Myxidiidae Family 2 Coccomyxidae (p. 658) Family 3 Myxosomatidae (p. 658) Family 4 Myxobolidae (p. 658)

Family

Myxidiidae Thelohan

Genus Myxidium Butschli (Cystodiscus Lutz). Spores fusiform with

pointed or rounded ends; polar filament comparatively long,
coelozoic or histozoic in fishes, also in amphibians
fine;

and

reptiles.

Nu-

merous

species.
a, b;

M.

lieberkuhni Butschli (Figs. 70,

284, a-d). In urinary blad-

der of Esox spp.; spores 18-20/z

distributed. Development (Cohn, 1896; Debaisieux, 1916); division (Kudo, 1921a; Bremer, 1922). M. immersum (Lutz) (Cystodiscus immersus Lutz; M. lindoyense Carini). (Fig. 284, e, f). In the gall bladder of species of Bufo, Leptodactylus, Atelopus, etc.; in Brazil and Uruguay. Trophozoites circular to oval, and very thin; up to 4 mm. in diameter; disporo-

by 5-6 /x; widely

blastic; polysporous.

Spores

11. 8-13. 3m

by

7.5-8. 6m; shell-valves

650

PROTOZOOLOGY

marked with 1 longitudinal and 7-9 transverse ridges (Cordero, 1919; Kudo and Sprague, 1940). M. serotinum Kudo and Sprague (Figs. 282, f-h; 283). In the gall bladder of Bufo terrestris, Rana pipiens, R. clamitans and R. sphenocephala; in the United States. Trophozoites up to 6.5 by 1.8 mm.,
extremely thin; cytoplasm highly alveolated; endogenous budding; disporoblastic; polysporous. Spores 16-18ju by 9m; shell-valve with 2-4 longitudinal and 10-13 transverse ridges (Kudo, 1943).

Fig. 283. Scattered spores, young and sporulating trophozoites of Myxidium serotinum, as seen in the bile of a frog in life, X64 (Kudo).

M.

ozoites large disc-like

kudoi Meglitsch. In gall-bladder of Ictalurus furcatus; trophup to 1 mm. in diameter; spores 8.5-12/; long

by 4-6 m (Meglitsch, 1937). Genus Sphaeromyxa Thelohan. Spore fusiform, but ends usually
truncate; polar filament short, thick; trophozoites large, discoid;
coelozoic in marine fish. Several species.
S. balbianii T. (Figs. 70, e; 284, g-4).

and other marine

S. sabrazesi

fish in

Europe and

of

In gall-bladder of Motella Siphostoma in the United

j-Z).

States; spores 15-20/*

by 5-6 n (Naville, 1930). Laveran and Mesnil (Figs. 276; 277; 284,

In gall-

CNIDOSPORIDIA, MYXOSPORIDIA
bladder of Hippocampus, Motella,
baisieux, 1925; Naville, 1930).
etc.; spores

0. )7

22-28m by 3-4/z (Dein front view;

Genus Zschokkella Auerbach. Spore semi-circular

fusiform in profile; circular in cross-section; ends pointed obliquely;

Fig. 284. a-d,

e, f,

Myxidium

lieberkuhni

(a,

a trophozoite,

X220

(Lieber-

klihn); b, a small trophozoite,

h,

X1000; c, d, spores, X1400) (Kudo); M. immersum, X1400 (Kudo); g-i, Sphaero7?tyxa balbianii (g, X|;

a spore, X1400 (Davis); i, spore with extruded polar filaments, X840 (Thelohan)); j-1, S. sabrazesi (j, trophozoite, X10; k, 1, spores, X1000) (Schroder); m, n, Zschokkella hildae (m, X600; n, X1060) (Auerbach); o-t, Coccomyxa morovi (o, a young binucleate trophozoite; p-s, development of sporoblast; t, a spore with the extruded polar filament), X665 (Lger and Hesse).

polar capsules large, spherical; sutural line usually in S-form, coelozoic in fish or amphibians.

A few species.
Gadus
spp.;

Z. hildae A. (Fig. 284, m, n). In urinary bladder of

spores 16-29m

by 13-18m (Auerbach,

1910).

658

PROTOZOOLOGY
Family 2 Coccomyxidae Leger and Hesse

section;

Spore ellipsoidal; one polar capsule at one end; circular in crossundoubtedly a border-line form between Myxosporidia and

Microsporidia.

Genus Coccomyxa Leger and Hesse. Polar filament long, fine; and Hesse, 1907). C. morovi L. and H. (Fig. 284, o-t). In the gall-bladder of Clupea pilchardus; spores 14 n by 5-6 /x (Georgevitch, 1926).
coelozoic parasite in marine fish (Leger

Family 3 Myxosomatidae Poche

Two

or 4 polar capsules at anterior end; sporoplasm without any

circular,

iodinophilous vacuoles.

Genus Myxosoma Thelohan (Lentospora Plehn). Spore

at anterior end; histozoic in marine or fresh water
species.
fish.

oval or ellipsoid in front view, lenticular in profile; 2 polar capsules

Several

M.
1926).

catostomi

Kudo

(Figs. 58; 275).

tissue of Catostomus commersonii; spores 13-15/x

In the muscle and connective by 10-1 1.5^ (Kudo,

M.
drium

cerebralis (Hofer) (Fig. 285, a). In the cartilage

and perichon-

of salmonid fish;

young

fish

are especially affected

as the

by

in-

fection,

the disease being

known

"twist-disease" (Dreh-

krankheit); spores 6-10m in diameter, (p. 648). M. funduli Kudo. In the gills of Fundulus; spherical cysts
360/x

up
8/x

to

by 264^; spores pyriform,

14/x

by 8/x by

6/x;

polar capsules

by

2 M (Kudo, 1918).

Other species (Bond, 1938-1939).

Genus Agarella Dunkerly. Spore elongate oval; 4 polar capsules at anterior end; shell prolonged posteriorly into long processes. One
species.

A.
fish,

gracilis

D. (Fig. 285,

b).

In the testis of South American lung-

Lepidosiren paradoxa (Dunkerly, 1915, 1925).

Family 4 Myxobolidae Thelohan

One, 2, with an iodinophilous vacuole.
or 4 polar capsules grouped at anterior end; sporoplasm
Butschli. Spores ovoidal or ellipsoidal, flat-

Genus Myxobolus

tened; 2 polar capsules at anterior end; sporoplasm with an iodinophilous vacuole; sometimes with a posterior prolongation of shell;
exclusively histozoic in freshwater fish or amphibians.
species.

Numerous

M.

pjeifferi

Thelohan

(Fig. 285, e,f). In the

muscle and connective

CNIDOSPOPJDIA, MYXOSPORIDIA
tissue of

659

and B.
fish die

plebejus;

body and various organs of Barbus barbus, B. fluviatilis, tumor up to a diameter of 7 cm; most of infected from the effect (Keysselitz) spores 12-12. by. by 10-10. 5m.
;

M.

orbiculatus

Kudo

(Fig. 285, g-i).

In muscle of Notropis

gilberti;

spores 9-10m in diameter by 6.5-7m thick. conspicuus K. (Fig. 285, j, k). In corium of head of Moxostoma

breviceps;

tumors 1/2-4 mm.; spores

9-11.5/x

by 6.5-8m (Kudo,

1929).

Fig. 285. a, Myxosoma cerebralis, showing two views of spore, X800 (Plehn); b, a spore of Agarella gracilis, X1660 (Dunkerly); c, d, front and side views of fresh spores of Thelohanellus notatus, XI 530 (Kudo); e, f, Myxobolus pfeifferi (Keysselitz) (e, Part of section of a cyst; f, a spore treated with iodine solution, X 1 780) g-i, M. orbiculatus (Kudo) (g, infected host's muscle, X600; h, a fresh spore; i, Lugol-treated spore,
;

X1000); j, k, views of fresh spores of M. conspicuus, X1530 (Kudo); l-o, M. squamosus (1, a cyst under a scale, X6.5; m-o, views of fresh spores, XI 530); p-r, spores of Henneguya exilis, XI 530; s-u, spores of Unicauda clavicauda, X1530 (s, t, fresh spores; u, a stained spore without the process

(Kudo)).

660

PROTOZOOLOGY
intestinalis

M.

K.

(Fig.

I,

a).

In the intestinal wall of Pomoxis

sparoides; (fixed unstained) spores, 12-13/x

tological changes

by

10-12.5/x; the his-

brought about by this protozoan have been mentioned elsewhere (p. 27) (Kudo, 1929). M. squamosus K. (Fig. 285, l-o). In connective tissue below scales
Hybopsis kentuckiensis; spore circular in front view,
8-9/x in

of

diameter, 4.5-5m thick.

Genus Thelohanellus Kudo. Pyriform

freshwater
fish.

spores, each with one polar

capsule; sporoplasm with an iodinophilous vacuole; histozoic in

11 species (Kudo, 1933). (Mavor) (Figs. 1, 6; 285, c, d). In subdermal connective tissue of Pimephales notatus, Cliola vigilax, Notropis cornutus, N. blennius, and Leuciscus rutilus; tumor up to 7 mm. in diameter; spores 17-18m by 7.5-10m; host tissue surrounding the organism becomes so greatly changed that it appears as an epithelium (p. 31) (Debaisieux, 1925; Kudo, 1929, 1934). Genus Henneguya Thelohan (Myxobilatus Davis). Spore circular T. notatus

or ovoidal in front view; flattened; 2 polar capsules at anterior end;

each shell-valve prolonged posteriorly into a long process; sporoplasm with an iodinophilous vacuole; mostly histozoic in freshwater fish.

Numerous
H.
exiles

species.

Kudo

(Figs. 278; 285, p-r). In gills

and integument

of

Ictalurus punctatus; cysts

up

to 3

mm.

in diameter, conspicuous;

spores, total length 60-70/x, spore proper 18-20/x long

by

4-5/x

wide

by 3-3.5m thick (Kudo, 1929, 1934). H. mictospora Kudo. In the urinary bladder
Micropterus salmoides; spores
thick; caudal prolongation 30-40/x long.

of

Lepomis spp. and

13.5-15m long, 8-9m wide, 6-7.5m

Genus Unicauda Davis. The spore is similar to that of Henneguya, but the single caudal appendage is not an extension of the shellvalves. Several species (Davis, 1944).

tissue of the

U. clavicauda (Kudo) (Fig. 285, s-u). In the subdermal connective minnow, Notropis blennius; oblong or ellipsoid cysts,

1-1.5

mm.

in the longest diameter; spores 10.5-11. 5/x

by

8. 5-9. 5m

by

6m; appendage 20-30m

by 3-6.5m (Kudo,

1934).

Order 2 Actinomyxidia Stole

The Cnidosporodia placed

spore
is

in this order

have been

less

frequently

studied and, therefore, not so well

known

as the Myxosporidia.

The

enveloped by a membrane, or shell composed of 3 valves which are sometimes drawn out into simple or bifurcated processes. There are also 3 polar capsules in the spore and the polar filaments

CNIDOSPORIDIA, ACTINOMYXIDIA
are plainly visible

661

sporoplasms occur in each spore. In the fully grown stage, the body is covered by a membrane and contains eight sporoblasts which develop in turn into eight spores. Whether the pansporoblast is formed by union of two cells or not, is unknown. The nuclei and cytoplasm divide and isogamy takes place. The zygote thus formed is the sporont in which a single spore is produced by repeated nuclear division combined with cytoplasmic differentiation. The Actinomyxidia inhabit the body cavity or the gut-epithelium of fresh or salt water annelids. Taxonomy, morphology and developto

m vivo.

One

many

ment (Granata,

1925).

Spore with a double membrane; inner membrane a single piece, the outer trivalve; a single binucleate sporoplasm Family 1 Tetractinomyxidae Spore membrane a single trivalve shell; a single octonucleate sporoplasm or 8 uninucleate sporoplasms Family 2 Triactinomyxidae

Family

Tetractinomyxidae Poche

Genus Tetractinomyxon Ikeda. In the coelom of the sipunculid Petalostoma minutum; spores tetrahedron, without processes; trophospores.

rounded body, when mature; pansporoblast develops 8 Seemingly borderline forms between the Myxosporidia and the Actinomyxidia. T. intermedium I. (Fig. 286, a). Spherical pansporoblasts 20-25ju in diameter; spores 7-8ju in diameter; in coelom of the sipunculid,
zoite a

Petalostoma

minutum

(Ikeda, 1912).

Family 2 Triactinomyxidae

Genus Triactinomyxon
into a long process, the

Stole. Each of 3 shell-valves drawn out whole anchor-like; spore with 8 or more

uninucleate sporoplasms; in the gut-epithelium of oligochaetes.

T. ignotum S. (Fig. 286, d). Spore with 8 sporoplasms; in Tubifex
tubifex.

T.

magnum

Granata. Spore with 16 sporoplasms; in Limnodrilus

in

udekemianus.
T. legeri

Mackinnon and Adams. Spore with 24 sporoplasms;

Tubifex tubifex.
T. T. mrazeki

dubium Granata. Spore with 32 sporoplasms; in Tubifex tubifex. Mackinnon and Adams. Spore with 50 sporoplasms; in

Tubifex tubifex.
oligochaetes; spores rounded, without

Genus Sphaeractiroryxon Caullery and Mesnil. In the crelcm cf any processes; in early stage

G62

PROTOZOOLOGY
by a
bicells

of development, there are 2 uninucleate bodies surrounded

nucleate envelope; 2 inner

multiply into 16

cells

which unite
1

in

pairs; nucleus of zygote of sporont divides first into 2;

of the nu-

clei divides into 6 which form 3 shell-valves and 3 polar capsules, while the other nucleus together with a portion of cytoplasm remains

Fig. 286. a, Tetractinomyxon intermedium, X800 (Ikeda) b,; Sphaeradinomijxon stolci, X600 (Caullery and Mesnil); c, S. gigas, X665 (Granata); d, Triactinomyxon ignotum, X165 (L6ger); e, Hexactinomyxon psammoryctis, X300 (Stole); f, g, Synactinomyxon tubificis, X600 (Stole); eoactinomyxum globosum, XS60 (Granata); i, Cuyenotia sphaerulosa, h,

X2095

(Naville).

outside the envelope, and undergoes multiplication; multinucleate sporoplasm migrates into spore; sporoplasm later divides into a

number of uninucleate sporoplasms which, when spores gain entrance into a new host, begin development. S. stolci C. and M. (Fig. 286, b). Spore spherical; in Clitellis arelarge

narius and Hemitubifex benedii.

CNIDOSPORIDIA, ACTINOMYXIDIA
S. gigas

663
hoff-

Granata

(Fig. 286, c). In the

coelom of Limnodrilus

meisteri (Granata, 1925).

Genus Hexactinomyxon
H. psammoryctis

Stole.

Each

of 3 shell-valves prolonged

into 2 processes; spore appears as a

S. (Fig. 286, e).

6-armed anchor.
In the gut-epithelium of Psam-

moryctes barbatus; sporoplasm multinucleate.

Genus Synactinomyxon and 1 conical valve.

tubifex.

Stole.

Spore with 2 prolonged shell-valves

S. tubificis S. (Fig. 286, /, g). In the gut-epithelium of Tubifex

Genus Neoactinomyxum Granata. 3

cess,

shell-valves without

any pro-

distended to hemisphere.

N. globosum G. (Fig. 286, h). In the gut-epithelium of Limnodrilus udekemianus ; spore with numerous sporoplasms (Granata, 1925;
Jfrovec, 1940).

Genus Guyenotia

Naville. Pansporoblast with 8 spores; spore

drawn out posteriorly into digitiform process, longer than diameter of spore; sporoplasm with 32
spherical with 3 shell-valves, each
nuclei.

G. sphaerulosa

N.

(Fig. 286,

i).

In the gut-epithelium of Tubifex

40ju long.

tubifex; spores 15/x in diameter;

appendages of mature spore

References

Auerbach, M.:

(1912) Studien iiber die Myxosporidien der norwegischen Seefische und ihre Verbreitung. Zool. Jahrb. Syst., 34:1. Awerinzew, S.: (1913) Ergebnisse der Untersuchungen iiber parasitische Protozoen der tropischen Region Afrikas. III. Zool. Anz., 42:151. Bond, F. F. (1938) Cnidosporidia from Fundulus heteroclitus. Tr.
:

(1910) Die Cnidosporidien. Leipzig.

of

Am. Micr. Soc, 57:107. (1938a) The doubtful

Fundulus

relationship of Sporozoa to the ulcers

heteroclitus. J. Parasit.,

24:207.

(1939) The seasonal incidence of myxosporidian parasites infecting Fundulus heteroclitus. Tr. Am. Micr. Soc, 58:156. Bremer, H.: (1922) Studien iiber Kernbau und Kernteilung von Myxidium lieberkiihni Butschli. Arch. Protist., 45:273. Butschli, O.: (1881) Beitrage zur Kenntnis der Fischpsorospermien. Ztschr. wiss. Zool., 35:629. (1882) Myxosporidia. Bronn's Klassen und Ordnungen der Protozoa. 1:590. Carini, A.: (1932) Myxidium lindoyense n. sp., Rev. Biol. Hyg., 3:
83.

Caullery, M. and Mesnil,

myxidies.
I.

F.: (1905)

Recherches sur

les

Actino-

Arch. Protist., 6:272.

664

PROTOZOOLOGY

Cepede, C: (1906) Myxosporidies des poissons des Alpes Franchises. Ann. rUni. Grenoble, 18:57. Chakravarty, M.: (1939) Studies on Myxosporidia from the fishes
Arch. Protist., 92:169. Studies on Myxosporidia from the common food fishes of Bengal. Proc. Indian Acad. Sc, 18:21. and Basu, S. P.: (1948) Observations on some myxosporidians parasitic in fishes, etc. Proc. Zool. Soc. Bengal, 1:23. Cohn, L.: (1896) Ueber die Myxosporidien von Esox lucius und Perca fluviatilis. Zool. Jahrb. Anat., 9:227. Cordero, E. H.: (1919) Cystodiscus immersus Lutz: Mixosporidio de los batracios del Uruguay. Physis, 4:403. da Cunha, A. M. and da Fonseca, 0.: (1917-1918) Sobre os myxosporidios dos peixes brazileiros. I-IV. Brazil Medico, 31:321(1943)
32, 414.
of Bengal, etc.

Davis, H. S.: (1917) The Myxosporidia of the Beaufort region. Bull. U. S. Bureau Fish., 35:199. (1924) A new myxosporidian parasite, the cause of "wormy" halibut. Rep. U. S. Comm. Fisheries for 1923, App. 8. (1944) A revision of the genus Henneguya with descriptions of two new species. Tr. Am. Micr. Soc, 63:311.

Debaisieux,
lule,

P.: (1918) Notes sur le Myxidium lieberkiihni. La Cel30:281. (1924) Sphaeromy.va sabrazesi Laveran et Mesnil. Ibid., 35:

269. (1925) Etudes sur les Myxosporidies. III. Arch. zool. exper.
gen., 64:353.

Dunkerly,

J. S.:

(1915) Agarella gracilis, etc.

Proc. Roy. Phys.

Soc, 19:213.

(1921) Fish Myxosporidia from Plvmouth. Parasitology, 12: 328. (1925) The development and relationship of the Myxosporidia.

Quart.

J.

Erdmann, Rhoda:

Micr. Sc, 69:185. (1917) Chloromyxum leydigi

und

seine Bezieh-

ungen zu anderen Myxosporidien. Arch. Protist., 36:276. Fantham, H. B., Porter, Annie and Richardson, L. R, (1939) Some Myxosporidia found in certain freshwater fishes in Quebec Province, Canada. Parasitology, 31:1. (1940) Some more Myxosporidia observed in Canadian fishes. Ibid., 32:333. Fish, F. F.: (1939) Observations on Henneguya salminicola, etc
:

J. Parasitol., 25:169. Fujita, T.: (1912) Notes on

new sporozoan parasites of fishes. Zool. Anz., 39:259 (1923) Studies on Mvxosporidia of Japan. J. Coll. Agr. Sapporo, 10:191. (1924) Studies on myxosporidian infection of the crucian carp. Japan J. Zool., 1 45. (1927) Studies on Myxosporidia of Japan* J. Col. Agr. Sapporo, 16:229.
:

CNIDOSPORIDIA, ACTINOMYXIDIA
Georgevitch,
J.:

665
recueillie as

(1916)

Note sur

les

myxosporidies

Roscoff. Bull. soc. zool. France, 41:86. (1917) Recherches sur le developpement de Ceratomyxa herouardi. Arch. zool. exper. gen., 56:375. (1926) Sur la Coccomyxa de la sardine. Ibid., 65(N.-R):57. (1936) Nouvelles etudes sur les myxosporidies. Bull. l'Acad. Sc. Math. Natur. Belgrade, B, 3:87. Granata, L.: (1925) Gli Attinomissidi. Arch. Protist., 50:139. Guimaraes, J. R. A.: (1931) Myxosporideos da ichtiofauna brasileira. Fac. Med. Sao Paulo Thesis. 50 pp. Gurley, R. R. (1894) The Myxosporidia or psorosperms of fishes, etc. Rep. U. S. Fish. Comm., 26:65. Ikeda, I.: (1912) Studies on some sporozoan parasites of Sipuncu:

Arch. Protist., 25:240 loids. I. Jaczo, I.: (1940) Beitrage zur Kenntnis der Myxosporidien der Balaton-Fische. I. Arb. ungarisch. Biol. Forschungsinst., 12:
277.

Jameson, A. P.: (1913) A note on some Myxosporidia collected at Monaco. Bull, l'lnst. Ocean., 273:1. (1929) Myxosporidia from Californian fishes. J. Parasitol.,
16:59. (1931) Notes on California Myxosporidia. Ibid., 18:59. Jirovec, O. (1940) Zur Kenntnis einiger in Oligochaten parasitierenden Protisten. II. Arch. Protist., 94:212. Johnston, T. H. and Bancroft, M. J.: (1919) Some new sporozoan parasites of Queensland freshwater fish. J. Proc. Roy. Soc. N. S. Wales, 52:520. Keysselitz, G.: (1908) Ueber durch Sporozoen (Myxosporidien) hervorgerufene pathologische Veranderungen. Verh. Ges. deutsch. Natur. Aertze, 79:452. Kudo, R. R.: (1918) Contributions to the study of parasitic ProtoIV. J. Parasitol., 4:141. zoa. (1920) Studies on Myxosporidia. Illinois Biol. Monogr., 5: 245. (1921) On the nature of structures characteristic of cnidosporidian spores. Tr. Am. Micr. Soc, 40:59. (1921a) On some Protozoa parasitic in freshwater fishes of
:

New York. J. Parasitol., 7: 166. (1922) On the morphology and

tist.,

life

history of a myxosporid-

ian, Leptotheca ohhnacheri, etc. Parasitology, 14:221. (1926) On Myxosoma catotsomi Kudo, 1923, etc. Arch.

Pro-

56:90. (1929) Histozoic Myxosporidia found in freshwater fishes of Illinois. Ibid., 65:364. (1933) A taxonomic consideration of Myxosporidia. Tr. Am. Micr. Soc, 52:195. (1934) Studies on some protozoan parasites of fishes of Illinois. Illinois Biol. Monogr., 13:1. (1943) Further observations on the protozoan, Myxidium serotinum, etc. J. Morphol., 72:263.


666
(1944)
bilis

PROTOZOOLOGY
The morphology and development
of its host,

Kudo, and

of Noserna notaSphaerospora polymorpha Davis, etc.

Illinois Biol.

Monogr., 20:1.
V.: (1940)

and Sprague,
serotinum n. sp., Havana, 6:65.

On Myxidium immersum and M.

etc.

Rev. Med. Trop. Parasit. Bact. Clin. Lab.

L.: (1929) Une nouvelle maladie parasitaire funeste aux elevages de tanche, "la spherosporose." Trav. Lab. Hydr. Pise. Uni. Grenoble, 21:7. and Hesse, E.: (1907) Sur une nouvelle myxosporidie parasite de la sardine. C. R. Acad. Sc, 145:85. Lutz, A.: (1889) Ueber ein Myxosporidium aus der Gallenblase brasilianischer Batrachier. Centralbl. Bakt., 5:84. Mavor, J. W. (1915) Studies on the Sporozoa of the fishes of the St. Andrew's region. Ann. Rep. Dep. Marine Fish., 47 (Suppl.)

Leger,

25.

(1916) Studies on the protozoan parasites of the fishes of the Georgian Bay. Tr. Roy. Soc. Canada, Ser. 3, 10:63. Meglitsch, P. A.: (1937) On some new and known Myxosporidia
of the fishes of Illinois. J. Parasit., 23:467.

(1947) Studies on Myxosporidia from the Beaufort region.

Ibid.,

I.

33:265. (1947a) II.

Ibid.,

33:271.
la

Naville, A.: (1927) Le cycle chromosomique, reduction chromatique de Chloromijxum

fecondation et la

leydigi.

Ann.

Inst.

Ocean., 4:177. (1930) Recherches sur le sexualite chez les myxosporidies. Arch. Protist., 69:327. (1930a) Le cycle chromosomique d'une nouvelle actinomyxidie: Guyenotia sphaerulosa n. g., n. sp. Quart. J. Micr. Sc, 73:
547.

Nemeczek,

A.: (1926) Beitrage zur Kenntnis der Myxosporidienfauna Brasiliens. Arch. Protist., 54:137. Nigrelli, R. F.: (1946) Parasites and diseases of the ocean pout, Macrozoarces americanus. Bull. Bingham Ocean. Collect., 9: 187. Noble, E. R.: (1939) Myxosporidia from tide pool fishes of California. J. Parasit., 25:359.

(1941) On distribution relationships between California tide pool fishes and their myxosporidian parasites. Ibid., 27:409. (1941a) Nuclear cycles in the life history of the protozoan genus Ceratomyxa. J. Morphol., 69:455. (1944) Life cycles in the Myxosporidia. Quart. Rev. Biol., 19:213. Parisi, B.: (1912) Primo contributo alia distribuzione geografica dei missosporidi in Italia. Atti. Soc. Ital. Sc. Nat., 50:283. Petruschewsky, G. K.: (1932) Zur Systematik und Cytologie der Myxosporidia aus einigen Fischen des Weissen Meeres. Arch. Protist., 78:543. Pinto, C: (1928) Myxosporideos e outros protozoarios intestinaes de peixes observados na America do Sul. Arch. Inst. Biol. Sao Paulo, 1:1.

CNIDOSPORIDIA, ACTINOMYXIDIA
Prehn, Marianne: (1904) Ueber

667

die Drehkrankheit der Salmoniden. Arch. Protist., 5:145. (1925) Eine neue Schleienkrankheit. Fisch.-Zeit., 28:299. Rice, V. J. and Jahn, T. L.: (1943) Myxosporidian parasites from the gills of some fishes of the Okoboji region. Proc. Iowa Acad. Sc, 50:313. (1943a) Internal myxosporidian infections of some fishes of Okoboji region. Ibid.,* 50:323. Schroder, O.: (1907) Beitrage zur Entwicklungsgeschichte der Myxosporidien, Sphaeromyxa sabrazesi. Arch. Protist., 9:359. Southwell, T. and Prashad, B.: (1918) Parasites of Indian fishes, etc. Rec. Indian Mus., 15:341. Thelohan, P.: (1892) Observation sur les myxosporidies et essai de classification de ces organisms. Bull. Soc. Philom., 4:165. (1895) Recherches sur les myxosporidies. Bull. Sc. Fr. Belg., 26:100. Ward, H. B.: (1919) Notes on North American Myxosporidia. J. Parasitol, 6:49. Willis, A. G.: (1949) On the vegetative forms and life history of Chloromyxum thyrsites Gilchrist and its doubtful systematic position. Australian Jour. Sc. Res., Ser. B. Biol. Sc, 2:379.

Chapter 29

Order 3 Microsporidia Balbiani

more widely distributed as parasites phyla than the Myxosporidia. They are however typically parasites of arthropods and fishes. All Microsporidia invade and undergo asexual division and sporogony within the host cell. These infected cells may show frequently an enormous
are far

Microsporidia THE among various animal

Fig. 287. Effects of microsporidian infections upon host animals, a, the central nervous system of Lophius piscatoris infected by Nosema lophii (Doflein); b, a smelt infected by Glugea hertwigi, Xf (Schrader); c, a Culex larva infected by Thelohania opacita, X14 (Kudo); d, a Simulium

larva infected by T. multispora, X10 (Strickland); e, portion of testis of Barbus barbus infected by Plistophora longifdis, X1.4 (Schuberg); f, g, normal and hypertrophied nuclei of the adipose tissue cells of larval Culex pipiens, the latter due to a heavy infection by StempelKa magna,

X1330 (Kudo).
hypertrophy
of both the cytoplasmic body and nuclei (Figs. 287, /, g; 290, a-e), a characteristic feature of the host reaction toward this

particular group of protozoan parasites.

The microsporidian spore is on the whole relatively small as compared with that of Myxosporidia. In the vast majority it measures 3-6/i in the largest diameter. The chitinous spore membrane which is apparently of a single piece except in a few species, envelops the
668

MICROSPORIDIA

669

sporoplasm and the polar filament, a very long delicate filament. The latter may be enclosed within a polar capsule as in a myxosporidian spore. Structure of microsporidian spores (Leger and
Hesse, 1916a; Kudo, 1920, 1921, 1924b; Kohler, 1921).

When such spores are taken into the digestive tract of a specific host (Fig. 288), the polar filaments are extruded and perhaps anchor the spores to the gut-epithelium (a). The sporoplasms emerge as
amoebulae through the opening after the filaments become completely detached (b). By amoeboid movements they penetrate through the intestinal epithelium and enter the blood stream or body cavity and reach the specific site of infection (c). They then enter the

Fig. 288. The life-cycle of Stempellia magna, XS00 (Kudo), a, b, germination of spore in the mid-gut of culicine larva; c-k, division stages; 1-p, sporont formation; q-t, formation of 1, 2, 4, and 8 sporoblasts;
u, sporoblast; v-x,

development

of sporoblast into spore.

host cells and undergo multiplication at the expense of the latter {dn).

The trophozoites become sporonts (o), each of which produces a number of spores (p-x) characteristic of each genus. Some spores seem to be capable of germinating in the same host body, and thus the number of infected cells increases. When heavily infected, the host animal dies as a result of the degeneration of enormous numbers
of cells thus attacked.

Such

fatal infections

may occur in an epidemic

silkworms

form, as

is

well

known

in the case of the pebrine disease of

070
(Pasteur,

PROTOZOOLOGY
1870; Stempell,

1909; Kudo, 1916; Hutchinson, 1920; Jameson, 1922), Nosema-disease of honey bees (Zander, 1911; White, 1919; Farrar, 1947), microsporidiosis of mosquitoes (Kudo, 1921-1930), etc. Taxonomy (Leger and Hesse, 1922; Kudo, 1924b; Jfrovec, 1936; Weiser, 1947); the polar filament (Kudo, 1913, 1918, 1924b; Morgenthaler, 1922; Ohshima, 1927, 1937). The Microsperidia are subdivided into two suborders:

Spore with a single polar filament Spore with 2 polar filaments

Suborder 1 Monocnidea Suborder 2 Dicnidea

(p.
(p.

070) 078)

Suborder

Monocnidea Leger and Hesse

Spore oval, ovoid, or pyriform, if subcylindrical length less than 4 times Family 1 Nosematidae breadth Family 2 Coccosporidae (p. 070) Spore spherical or subspherical Spore tubular or cylindrical, width less than 1/5 length, straight or curved Family 3 Mrazekiidae (p. 070)

Family

Nosematidae Labbe
single spore.

The majority of Microsporidia belong to this family. Genus Nosema Nageli. Each sporont develops into a Numerous species.

N. bombycis N. (Fig. 289, a, b). In all tissues of embryo, larva, pupa and adult of Bombyx mori; spores 3-4/z by 1.5-2/z, polar filament 57-72/z long when extruded; advanced infection is characterized by numerous minute brownish-black spots scattered over the body surface, which gave rise to such names as pebrine disease (France), Fleckenkrankbeit (Germany), Biriushi-Bio (Japan), Cota
(India), etc. (Fig. 289, b) to the disease; heavily infected larvae can-

not spin cocoon and perish; the organisms invade, and develop in, ova so that newly hatched larvae are already infected with this microsporidian. Viable spores introduced per os bring about infections
in Arctia caja (Stempell, 1909),

Margarnia

pyloalis, Chilo simplex

(Ohshima, 1935), and Hyphantria cunea (Kudo and DeCoursey,

Morphology and Development (Stempell, 1909; Kudo, 1924b). N. bryozoides (Korotneff) (Fig. 289, c, d). In the germ cells and cavity of the bryozoans, Plumatella fungosa and P. repens; spores 7-10/x by 5-6 M (Braem, 1911; Schroder, 1914). N. apis Zander (Fig. 289, e-g). In the mid-gut of honey bees; spores 4-6^ by 2-4 n; the extruded filament shows often 2 sections of differ1940).

ent undulations (Fig. 289, g) (Kudo, 1921a). The infection is confined to the digestive system, but the ovary of an infected queen bee

undergoes various degrees

of the

of degeneration depending on the extent gut infection (Fyg, 1945; Farrar, 1947; Hassanein, 1951),

MICROSPORIDIA
though the eggs are free from the parasites, which condition may be looked upon as a parasitic castration. Morphology and development

Fantham and Porter, 1912). N. cyclopis Kudo (Fig. 289, h, i). In Cyclops fuscus; spores 4.5/z by 3 M (Kudo, 1921b). N. anophelis K. (Fig. 289, j, k). In the larvae of Anopheles quadrimaculatus; spores 5-6 m by 2-3^ (Kudo, 1925). It was also found in A.
(Zander, 1909;

maculipennis (Missiroli, 1928).

Fig. 2S9. a, b, Nosema bombycis (Kudo) (a, fresh spores, X1500; b, a heavily infected silkworm larva showing characteristic dots on integument, Xf); c, d, N. bryozoides (c, infected funiculus, X270 (Braem); d, a stained spore, X1200 (Schroder)); e-g, Ar apis (Kudo) (e, a fresh spore; f, a stained spore, X 1560; g, a spore with the extruded polar filament as seen in dark field, X800); h, i, views of fresh spores of N. cyclopis, X1560 (Kudo); j, k, fresh spores of N. anophelis, X1600 (Kudo); 1, m, preserved and stained spores of N. aedis, XI 530 (Kudo); n, Frenzelina conformis, a gregarine, infected by schizonts and spores of Nosema frenzelinae (Leger and Duboscq) o-q, Nosema notabilis, X 1400 (Kudo) (o, a stained trophozoite of Sphaerospora polymorpha, a myxosporidian, infected by six trophozoites of Nosema notabilis; p, another host trophozoite in which nine spores and two trophozoites of N. notabilis occur; q, six fresh spores
. ;

of

N.

notabilis).

672

PROTOZOOLOGY
aedis K. (Fig. 289,
I,

N.

m). In the adipose tissue of a larval Aedes

aegypti; spores broadly pyriform

and measure

7.5-9/u

by 4-5^; polar

capsule large; uninucleate sporoplasm posterior (Kudo, 1930).

N. frenzelinae Leger and Duboscq

gastric

(Fig. 289, n).

In the cytoplasm

of the cephaline gregarine, Frenzelina conformis, parasitic in the

caeca and intestine of Pachygrapsus marmoratus ; spores about 2.8m long; extruded polar filament up to 25/z long (Leger and Duboscq, 1909).

N.

notabilis

Kudo

(Fig. 289, o-q).

In the trophozoite of the myxo-

which inhabits the urinary bladder of Opsanus tau and 0. beta. The host fish remain free from the microsporidian infection. The entire development takes place in the cytoplasm of the host trophozoites. Trophozoites small binucleate, multiply by binary fission. Spores ovoid to ellipsoid; sporoplasm binucleate; fresh spores 2.9-4/z by 1.4-2.5/x; extruded polar filament 45-62//. When heavily infected, the host myxosporidian trophozoites degenerate and disintegrate. A unique example of hyperparasitism in which two cnidosporidians are involved (Kudo,
sporidian, Sphacrospo?'a polymorpha (p. 653)
1944).

Genus Glugea Thelohan. Each sporont develops

into 2 spores;

the infected host cells become extremely hypertrophied, and trans-

form themselves into the so-called Glugea cysts (Figs. 287, b; 290, e). Many species (Kudo, 1924b). G. anomala (Moniez) (Fig. 290, a-f). In Gasterosteus aculeatus, G. pungitus (sticklebacks) and Gobius minutus; cysts conspicuous, up to about 5 mm. in diameter; host cells are extremely hypertrophied; spores 4-6 m by 2-3 ju. Morphology and sporogony (Stempell, 1904;
Weissenberg, 1913; Debaisieux, 1920).
G. miilleri Pfeiffer. In the muscles of
locusta; spores 5-6 m

Gammarus
1919).

pulex and G.

by 2-3 ju (Debaisieux,

G. hertwigi Weissenberg (Figs. 287, b; 290, g, h). In the smelt, Osmerus mordax and 0. eparlanus. Schrader (1921) found the intestine the primary site of infection, the cysts varying in size, up to 3 mm. in diameter; as the cysts grow in the mucosa, they come to lie immediately under the peritoneum. Spores measure 4-5. 5/x by 22.5m- Fantham, Porter and Richardson (1941) found the cysts in the serous membrane of the hind gut; as the spores were 3.5-4.6^ by 1.5-2/z, they named the organism Glugea hertwigi var. canadensis. Morphology and spore-formation (Weissenberg, 1911, 1913; Schrader, 1921).

Genus Perezia Leger and Duboscq. Each sporont produces 2

MICROSPORIDIA
few species.
P. mesnili Paillot (Fig. 290,
?)

673

spores as in Glugea, but infected host cells are not hypertrophied.

In cells of silk glands and Malpi-

Fig. 290. a-f, Glugea anomala

tissue cell of the intestine of a

(a, a young trophozoite young host fish, seven days

in a

connective

after feeding on

spores; b,

c,

more advanced

multinucleated and 41/x in diameter,

stages; d, a later stage, the host cell being X1000 (Weissenberg) e, section of
;

an infected Gasterosteus aculeatus, showing two large cysts (Thedohan);

f,

a fresh spore, X1500 (Stempell)); g, h, G. hertwigi (Schrader) (g, crosssection of the infected intestine of a smelt, X14; h, 2 spores); i, stained spores of Perezia mesnili, X2265 (Palliot); j, section of Lankesteria ascidiae, a gregarine, infected by P. lankesteriae, X900(Leger and Duboscq) k-o, Gurleya tetraspora (k, infected hypodermal cells of Moina, X660 (Jirovec); 1, a mature sporont; m, a fresh spore (Doflein); n, stained
o, spores with extruded polar filaments (Jirovec)); p, q, a sporont and a spore with the extruded filament of Gurleya richardi, XT 200

spores;

(Cepede).

674

PROTOZOOLOGY
3.4/*

ghian tubules of larvae of Pieris brassicae; spores

(Paillot, 1918, 1929).

by

1.5-2/*

P. lankesteriae Leger and

Duboscq

(Fig. 290, j).

In the cytoplasm

of the gregarine, Lankesteria ascidiae, parasitic in the intestine of the

tunicate, Ciona intestinalis. It attacks only the gregarine

free in the

lumen

of the gut; the host nucleus does not

2.5/* long.

which are undergo hy-

pertrophy; ovoid spores

Genus Gurleya Doflein. Each sporont develops into four sporoblasts and finally into four spores. A few species. G. tetraspora D. (Fig. 290, k-o). In the hypodermal cells of Daphnia maxima and Moina rectirostris ; spores pyriform, 2.8-3.4/* by 1.4-1.6/* (Jfrovec, 1942). The infected host appears opaque white. G. richardi Cepede (Fig. 290, p, q). In Diaptomus castor; spores 46/* by 2.8/*. Genus Thelohania Henneguy. Each sporont develops into 8 sporoblasts and ultimately into 8 spores; sporont membrane may degenerate at different times during spore formation.
T. legeri

Numerous

species.

Hesse (T.

illinoisensis

Kudo)

(Figs. 76; 291, a-e). In the

fat bodies of the larvae of several species of Anopheles; spores 4-6/*

by

3-4/*; heavily infected larvae die

without pupation; widely

dis-

tributed. Spore-formation (Kudo, 1924).

T. opacita

Kudo

(Figs. 287, c; 291, /, g). In the adipose tissue of

the larvae of Culex mosquitoes; spores 5.5-6/* by 3.5-4/* (Kudo,

1922, 1924a).
T. reniformis
cells of

Kudo and Hetherington

(Fig. 291, h). In the gut

the nematode, Protospirura muris, in mice; reniform spores

3-4/*

by 1.5-1.8/* (Kudo and Hetherington, 1922). Genus Stempellia Leger and Hesse. Each sporont produces 1, 2, 4, or 8 sporoblasts and finally 1, 2, 4, or 8 spores. 2 species. S. magna Kudo (Figs. 287, /, g; 288; 291, i-l). In fat-bodies of various culicine larvae; spores 12.5-16.5/* by 4-5/*; polar capsule visible in life; polar filament when extruded under mechanical pressure measures up to 350-400/* long (Kudo, 1925a). Genus Duboscqia Perez. Sporont develops into 16 sporoblasts and
finally

16 spores. Host-cell nuclei extremely hypertrophied.

One

species.

D.

legeri P. (Fig. 291,

m-o). In the fat-body

cells of Reticulitermes

lucifugus

and

R.flavipes. Trophozoites invade the peri-midintestinal

cells

adipose tissue

which become enlarged into "cysts," up to

660/*

because of active multiplication of the organisms; each binucleate schizont becomes a sporont which grows and produces 16

by

300/*,

spores. Spores ovoid to ellipsoid; fresh spores are 4.3-5.9/*

by

2.2-3/*;

If 0M

m
/

Fig. 291. a-e, Thelohania legeri, X1570 (Kudo) (a, b, stained sporogonic stages; c, d, mature sporonts; e, a fresh spore); f, g, mature octosporous and tetrasporous sporonts of T. opacita, X1570 (Kudo); h, gut epithelial cells of Protospirura infected by T. reniformis, X1040 (Kudo and Hetherington) i-1, Stempellia magna, XI 570 (Kudo) (i, j, fresh spores; k, slightly pressed spore in Lugol; 1, a spore with the nearly completely extruded polar filament, stained after Fontana); m-o, Duboscqia legeri (Kudo) (m, the mid-gut of Reticulitermes flavipes with an enlarged and two uninfected fat bodies, X57; n, portion of an infected and two uninfected fat body cells of the termite in section; o, mature sporont in life, XI 530); p, q, Trichoduboscqia epeori (Leger) (p, a mature sporont, X1330; q, a fresh spore, X2670); r, s, stained spores of Plistophora longifilis, XI 280 (Schuberg).
;

G7G

PROTOZOOLOGY

sporoplasm uninucleate; extruded polar filament 80-95/x long (Perez,

1908; Kudo, 1942).

Genus Trichoduboscqia Leger. Similar

to Duboscqia in

number

of

spores produced in each sporont; but sporont with 4 (or 3) rigid transparent prolongations, difficult to see in life. One species.
T. epeori L. (Fig. 291, p, q). In fat-bodies of nymphs of the mayEpeorus torrentium and Rhithrogena semicolorata; sporonts

flies,

spherical, 9-10/* in diameter, with usually 16 spores; prolongations of

membrane

in sporont, 20-22/* long; spores pyriform, 3.5-4/* long

(Leger, 1926).

(often

Genus Plistophora Gurley. Sporont develops into variable number more than 16) of sporoblasts, each of which becomes a spore.

Several species.

P. longifilis Schuberg (Figs. 287, e; 291, r, s). In the testis of Barbus fluviatilis; spores 3/x by 2/i to 12/i by 6/*; extruded polar filament up to 510^ long. P. kudoi Sprague and Ramsey. In the epithelial cells of the midgut of Blatta orientalis; fresh spores about 3.2/* by 1.75/*; polar fila-

ment 25-50/* long. Genus Pyrotheca Hesse. Schizogony and sporogony unknown;
spores elongate pyriform, anterior end attenuated, posterior end rounded, slightly curved; sporoplasm in posterior region, with 1-2
nuclei; polar capsule large.

One

species (Hesse, 1935).

P. incurvata H. (Fig. 292,

a, b).

In fat-bodies and haemocoele of

polar filament 130/* long.

Megacylcops

viridis; spores 14/*

by

3/*;

Family 2 Coccosporidae Kudo

Genus Coccospora Kudo (Cocconema Leger and Hesse). Spore

spherical or subspherical. Several species (Leger

and Hesse, 1921,

1922; Kudo, 1925b).

C. slavinae (L.

and H.)

(Fig. 292,
3/* in

c,

d).

In gut-epithelium of Slavina

appendiculata; spores about

diameter.

Family 3 Mrazekiidae Leger and Hesse

Genus Mrazekia L. and H. (Myxocystis Mrazek). Spore, tubular and straight; a long or short process at one extremity (Leger and
Hess, 1916). Species (Jfrovec, 1936a).

M.

caudata L. and H. (Fig. 292,

e,

/).

In the lymphocytes of

Tubifex tubifex; spore cylindrical, 16-18/* by 1.31.4/*, with a longprocess.

ess;

Genus Bacillidium Janda. Spore cylindrical, but without any procone end narrowed in a few species (Janda, 1928). Several species

(Jfrovec, 1936a).

MICROSPORIDIA

G77

B. eriodrili J. (Fig. 292, g). In the lymphocytes in the posterior portion of the body cavity and nephridia of Criodrilus lacuum; infected lymphocytes

become hypertrophied from

15/* to

200-400/* in

diameter; the infected part of the body appears yellowish; spores

20-22/*

by 1/* (Janda); 15.5-17/* by 1.2-1.4/* up (commonly 18-20/* by 1.4-1.5/*) (Jirovec).

to 24-25/*

by 1.6m

Fig. 292. a, b, stained spores of Pyrotheca incurvata, X1330 (Hesse); the latter with extruded filament, d, spores of Coccospora slavinae, XI 330 (Leger and Hesse); e, f, Mrazekia caudata (e, an infected host cell, X465 (Mrazek); f, a spore, XI 165 (L6ger and Hesse)); g, Criodrilus lacuum, infected by Bacillidium eriodrili, showing the enlarged posterior region, Xf (Janda); h, i, B. limnodrili (Jirovec) (h, trophozoites and spores of the microsporidian in a host lymphocyte, X600; i, a stained spore, X930); j, k, stained spores of Cougourdella magna, XI 330 (Hesse);
c,
1,

a spore of Octospora muscae-domesticae, X1430 (Chatton and Krempf); m, n, spores of Spiroglugea octospora (L6ger and Hesse) (m, X665; n, X2000); o, p, spores of Toxoglugea vibrio (Leger and Hesse) (o, X665; p, X2000) q, stained spores of T. gerridis, X2000 (Poisson) r, s, a fresh and a stained spore of Telomyxa glugeiformis, X2000 (Leger and Hesse).
; ;

B. limnodrili Jirovec (Fig. 292,

of

h, i). In lymphocytes within gonads Limnodrilus claparedeanus ; spores 22-24/* by 1.5/* (Jfrovec,

1936a).

Genus Cougourdella Hesse. Spore

(Hesse, 1935).
C.

cylindrical,

with an enlarged
3 species
of

extremity, resembling the fruit of Lagenaria cougourda.

magna H.

(Fig. 292, j, k). In

haemocoele and fat body

Mega-

678

PROTOZOOLOGY

cyclops viridis; spores 18m by 3m; polar filament 110m long; sporoplasm with 1-2 nuclei or 2 uninucleate sporoplasms.

Genus Octosporea Flu. Spore cylindrical; more or less curved; ends similar. 6 species (Jirovec, 1936a). 0. muscae-domesticae F. (Fig. 292, I). In gut and germ cells of Musca and Drosophila; spores 5-8 m long (Chatton and Krempf,
1911).

Genus Spiroglugea Leger and Hesse. Spore tubular and spirally One species. S. octospora L. and H. (Fig. 292, m, n). In fat body of larvae of Ceratopogon sp.; spores 8-8. 5m by 1/x. Genus Toxoglugea (Toxonema) Leger and Hesse. Minute spore
curved; polar capsule large.

curved or arched in semi-circle. 4 species (Poisson, 1941). T. vibrio L. and H. (Fig. 292, o, p). In the fat body of Ceratopogon
sp.; spores 3.5m

by

less

than

0.3ju.

T. gerridis Poisson (Fig. 292,

q).

In the fat body of the bug,

Aquarius najas; sporont gives rise to eight sporoblasts and then to eight spores; also monosporous; microspores 4.5m by 0.8m, the polar filament 40-50m long; macrospores 7-8m long.
Suborder 2 Dicnidea Leger and Hesse

Family Telomyxidae Leger and Hesse

Genus Telomyxa Leger and Hesse. Spore with 2 polar capsules; sporont develops into 8, 16, or more sporoblasts and finally 8, 16, or more spores (Leger and Hesse, 1910). Four species (Poisson, 1941). T. glugciformis L. and H. (Fig. 292, r, s). In the fat body of the larva of Ephemera vulgata; spores 6.5m by 4m.
Order 4 Helicosporidia Kudo
This order has been created to include the interesting organism, Helicosporidium, observed by Keilin. Although quite peculiar in the
structure of
its

spore, the organism seems to be best placed in the

Cnidosporidia.

The minute spore is composed of a thin membrane of one piece and of three uninucleate sporoplasms, around which is coiled a long thick filament. Young trophozoites are found in the host tissues or body cavity. They undergo schizogony, at the end of which uninucleate sporonts

become

differentiated.
cells

sporont divides apparently

twice and thus forms four small

which develop into a spore.

The complete

life-history

is still

unknown.

Genus Helicosporidium

Keilin. Parasitic in arthropods; schizog-

HELICOSPORIDIA

679

illustrating the probable development of Helico1600 (Keilin). a-c, schizont and schizogony; d, sporont(?); e, three stages in formation of four-celled stage; f, hypothetical stage; g, young spore before the spiral filament is formed; h, mature spore; i, j, opening of spore and liberation of sporoplasms. a-h, in living host larva; i, j, in dead host body.

Fig. 293.

Diagram

sporidia,

X about

ony and sporogony; spore with central sporoplasms and a single thick coiled filament. One species (Keilin, 1921). H. parasiticum K. (Fig. 293). In body cavity, fat body, and nervous tissue of larvae of Dasyhelea obscura and Myceiobia pallipes (Diptera), and Hericia hericia (Acarina), all of which inhabit wounds of elm and horse-chestnut trees; schizonts minute; spores 5-6/x in diameter; extruded filament 60-65/* by 1/z thick.
References

Borchert, A.: (1930) Nosemainfektion. Arch. Bienenk., 11:1. Braem, F.: (1911) Beitrage zur Kenntnis der Fauna Turkestans. VII. Trav. Soc. Imp. Nat., St. Petersbg., 42:1. Chatton, E. and Krempf, A.: (1911) Sur le cycle evolutif et la po-

680
sition

PROTOZOOLOGY

systematique des protistes du genre Octosporea, etc. Bull. soc. zool. France, 36:172. Debaisieux, P.: (1919) Etudes sur les microsporidies. II, III. La
Cellule, 30:153. (1920) IV. Ibid., 30:215.

(1928)
Ibid.,

Etudes cytologiques sur quelques microsporidies.

38:389.
F.: (1898) Studien zur Naturgeschichte der Protozoen.

Doflein,

III. Zool.

Jahrb. Anat., 11:281.

Fantham, H. B. and Porter, Annie: (1912) The morphology and life history of Nosema apis, etc. Ann. Trop. Med. Parasitol., 6:
163.

and Richardson, L.
in certain fishes

R.: (1941)

Some Microsporidia
Canada. Para-

found

and

insects in Eastern

sitology, 33:186. Farrar, C. L.: (1947)

losses in package bees as related to yields. J. Econ. Entom., 40:333. FoA, Anna: (1924) Modificazione al ciclo morfologico e biologico del Nosema bombycis Nageli. Boll. Lab. Zool. Gen. Agr., Portici,

Nosema

queen supersedure and honey

Fyg, W.

17:147. (1945) Die Einfluss der Nosema-Infektion auf die Eierstocke der Bienenkonigin. Schweiz. Bien.-Zeit., 68:67. Hassanein, M. H.: (1951) Studies on the effect of infection with Nosema apis on the physiology of the queen honey-bee. Quart. J. Micr. Sc, 92:225. Hesse, E.: (1904) Thelohania legeri n. sp., microsporidie nouvelle, parasite des larves d' Anopheles maculipennis Meig. C. R. soc. biol., 57:570. (1904a) Sur le developpement de Thelohania legeri. Ibid., 57:
:

571. (1935) Sur quelques microsporidies parasites de Megacyclops viridis. Arch. zool. exper. gen., 75:651. Hutchinson, C. M.: (1920) Pebrine in India. Mem. Dept. Agr. India, 1:177. Jameson, A. P. (1922) Report on the diseases of silkworms in India. Superint. Gov. Print., Calcutta, India. 165 pp.
:

(1928) Ueber Microorganismen aus der Leibeshohle von Criodrilus lacuum Hoffm. und eigenartige Neubildungen in der Korperwand dieses Tieres. Arch. Protist., 63:84. Jirovec, O.: (1936) Studien iiber Microsporidien. Mem. Soc. Zool. Tehee. Prague, 4:1. (1936a) Zur Kenntnis von in Oligochaten parasitierenden

Janda, V.

Microsporidien aus der Familie Mrazekiidae. Arch. Protist., 87:314. (1942) Zur Kenntnis einiger Cladoceren-Parasiten. II. Zool. Anz., 140:129. Keilin, D.: (1921) On the life-history of Helicosporidium parasiti-

cum
Kohler,

n. g., n. sp., etc. Parasitology, 13:97.

A.: (1921) Ueber die chemische Zusammensetzung der Sporenschale von Nosema apis. Zool. Anz., 53:85.

HELICOSPORIDIA
Korotoneff,
A.: (1892)

681
wiss.

Myxosporidium bryozoides. Ztschr.

ZooL, 53:591.

Kudo, R. R.:

(1913) Eine neue

Methode

die

Sporen von Nosema

bombycis Nageli mit ihren ausgeschnellten Polfaden dauerhaft zu praparieren, etc. Zool. Anz., 41:368. (1916) Contribution to the study of parasitic Protozoa. II.

Exp. St., 1:31. (1918) Experiments on the extrusion of polar filaments of cnidosporidian spores. J. Parasitol., 4:141. (1920) On the structure of some microsporidian spores. Ibid., 6:178. (1921) Studies on Microsporidia, with special reference to those parasitic in mosquitoes. J. Morphol., 35:123. (1921a) Notes on Nosema apis. J. Parasitol., 7:85. (1921b) Microsporidia parasitic in copepods. Ibid., 7:137. (1921c) On the nature of structures characteristic of cnidosporidian spores. Tr. Am. Micr. Soc, 40:59. (1922) Studies on Microsporidia parasitic in mosquitoes. II. J. Parasitol., 8:70. (1924) III. Arch. Protist., 49:147. (1924a) VI. Jour. Parasit., 11:84. (1924b) A biologic and taxonomic study of the Microsporidia. Illinois Biol. Monogr., 9:79. (1925) Studies on Microsporidia parasitise in mosquitoes. IV. Centralbl. Bakt. Orig., 96:428. Biol. Bull., 48:112. (1925a) V. (1925b) Microsporidia. Science, 61:366. (1942) On the microsporidian, Duboscqia legeri, parasitic in Reticulitermes flavipes. J. Morphol., 71:307. (1944) Morphology and development of Nosema notabilis, etc. Illinois Biol. Monogr., 20:1. and DeCoursey, J. D.: (1940) Experimental infection of Hyphantria cunea with Nosema bombycis. J. Parasitol., 26: 123. and Hetherington, D. C. (1922) Notes on a microsporidian parasite of a nematode. Ibid., 8:129. Labbe, A.: (1899) Sporozoa. Das Tierreich, Lief. 5, 180 pp. Leger, L.: (1926) Sur Triehoduboscqia epeori Leger. Trav. Lab. Hydro. Pise, 18:1. and Duboscq, O. (1909) Microsporidie parasite de Frenzelina. Arch Protist., 17:117. (1909a) Perezia lankesteriae, etc. Arch. zool. exper.
Bull. Seric.

and Hesse,
C.R.Acad.

1(N.-R):89.

E. (1910) Cnidosporidies des larves d'ephemeres. 150:411. (1916) Mrazekia, genre nouveau de microsporidies a spores tubuleuses. C. R. soc. biol., 79:345. (1916a) Sur la structure de la spore des microsporidies. Ibid., 79:1049. (1921) Microsporidies a spores spheriques. C. R. Acad. Sc, 173:1419.
:

Sc.,

682

PROTOZOOLOGY

(1922) Microsporidies bacteriformes et essai de systematique du group. Ibid., 174:327. Missiroli, A.: (1928) Alcuni protozoi parassiti dell' "Anopheles maculipennis." Riv. Malariol., 7:1. Morgenthaler, O. (1922) Der Polfaden von Nosema apis. Arch.
:

Bienenk., 4:53. Nageli, K. W. (1857) Ueber die neue Krankheit der Seidenraupe und verwandte Organismen. Bot. Zeit., 15:760. Ohmori, J.: (1912) Zur Kenntnis des Pebrine-Erreger, Nosema bombycis. Arb. kaiserl. Gesundh., 40:108. Ohshima, K. (1927) A preliminary note on the structure of the polar filament of Nosema bombycis, etc. Ann. Zool. Japan., 11:235. (1935) Infection of Chilo simplex by Nosema bombycis and function of the haemo-lymphocyte. J. Zool. Soc. Japan, 47:607. (1937) On the function of the polar filament of Nosema bombycis. Parasitology, 29:220. Paillot, A.: (1918) Deux microsporidies nouvelles parasites des chenilles de Pieris brassicae. C. R. Soc. biol., 81:66. (1929) Contribution a l'etude des microsporidies parasites de Pieris brassicae. Arch. d'Anat. Micros., 25:242. Pasteur, L.: (1870) Etude sur la maladie des vers a soie. Paris. Perez, C: (1908) Sur Duboscqia legeri, microsporidie nouvelle parasite du Termes lucifugus, etc. C. R. soc. biol., 65:631. Poisson, R.: (1941) Les microsporidies parasites des insectes hemipteres. IV. Arch. zool. exper. gen., 82(N.-R):30. Schrader, F.: (1921) A microsporidian occurring in the smelt. J. Parasitol., 7:151. Schroder, O.: (1914) Beitrage zur Kenntnis einiger Microsporidien. Zool. Anz., 43:320. Schuberg, A.: (1910) Ueber Mikrosporidien aus dem Hoden der Barbe und durch sie verursachte Hypertrophic der Kerne. Arb. kaiserl. Gesundh., 33:401. Sprague, V. and Ramsey, Juanita: (1942) Further observations on Plistophora kudoi, etc. J. Parasitol., 28:399. Stempell, W. (1904) Ueber Nosema anomalum. Arch. Protist., 4: 1. - (1909) Ueber Nosema bombijcis. Ibid., 16:281. Weiser, J. (1947) Klic k urcovani Mikrosporidii. Acta Soc. Sc. Nat.
:

Moravicae, 18:1.

Weissenberg, R.: (1911) Ueber

einige Mikrosporidien aus Fischen. Sitz.-ber Gesell. naturf. Freunde, Berlin, p. 344.

(1913) Beitrage zur Kenntnis des Zeugungskreises der Mikrosporidien, etc. Arch. mikr. Anat., 82:81. White, G. F.: (1919) Nosema-disease. Bull. U. S. Dept, Agr., No.
780.

Zander, E.: (1909) Tierische Parasiten

als Krankheitserreger bei der Biene. Leipz. Bienenz., 24:147. (1911) Krankheit und Schadlinge der erwachsenen Bienen. Handbuch der Bienenkunde. II. 42 pp.

Chapter 30

Subphylum
Ciliophora possess THE motion. In Suctoria the

2 Ciliophora Doflein
which serve as cell-organs of locoare present only during early develof this

cilia
cilia

opmental

stages.

The members

subphylum

possess a unique

organization not seen in the Plasmodroma; namely, except Protociliata, the Ciliophora contain two kinds of nuclei: the macronucleus and the micronucleus. The former is large and massive, and controls the metabolic activities of the organism, while the latter is minute and usually vesicular or less compact, and is concerned with the

reproductive processes. Nutrition

is

holozoic or parasitic; holophytic

is

in Cyclotrichium meunieri (p. 706). Sexual reproduction

mainly

by conjugation, and asexual reproduction

budding. The majority are free-living, forms also occur.

by binary fission or but a number of parasitic

is

The Ciliophora are divided

Cilia present

into

two

classes:

throughout trophic life Adult with tentacles; cilia only while young.
Class
1

Class 1 Ciliata Class 2 Suctoria (p. 863)

Ciliata

Perty

Protozoa of various habitats and body structures, though all possess cilia or cirri during the trophic stage. They inhabit all sorts of fresh and salt water bodies by free-swimming, creeping, or being attached to other objects; some are parasitic in other animals. Free-swimming forms are usually spherical to elliptical, while the creeping forms are, as a rule, flattened or compressed. The cilia are extremely fine, comparatively short, and as a rule arranged in rows (p. 55). In some forms they diminish in number and
class Ciliata includes

The

are replaced

by

cirri (p. 57).

The

cilia

are primarily cell-organs of lo-

comotion, but secondarily through their movements bring the food

matter into the cytostome. Moreover, certain cilia appear to be tactile organellae. The food of free-living ciliates consists of small plant and animal organisms which ordinarily abound in the water; thus their nutrition is holozoic. The ciliates vary in size from less than 10ju up to 2 mm. in large forms (as in an extended Spirostomum or Stentor). The cytoplasm is distinctly differentiated into the ectoplasm and the endoplasm. The ectoplasm gives rise to the cilia and trichocysts and is covered by a pellicle. The endoplasm contains nuclei, food vacuoles, contractile vacuoles, pigment granules, crystals, etc.
683

684

PROTOZOOLOGY

In the majority of ciliates, the anterior and posterior extremities are permanent and distinct; in all eytostome-possessing forms, the oral and aboral surfaces are distinguishable, while in numerous creeping forms the dorsal and ventral sides are differentiated. The body is covered by a very thin yet definite membrane, the pellicle, which is ordinarily uniformly thin and covers the entire body surface so closely that it is not recognizable in life. In some forms, such as Coleps, it develops into numerous platelets and in
others, such as Trichodina, into hook-like processes.

The outer

half

of the ectoplasm

may show
and

alveolar structure which, in section,

exhibits radiating
(p.

parallel lines. In this portion the

myonemes

61) are lodged.

The deeper

layer of the ectoplasm

is

structureless

and free from granules. In the ectoplasm are embedded the kinetosomes of cilia, which are arranged in longitudinal, oblique, or spiral rows. In recent years complex fibrillar systems have been recognized in many ciliates (p. 63-70). The cilia may fuse to form cirri, membranellae, and undulating membranes (p. 59) which occur
in certain groups. In

many euciliates

contractile vacuoles with one to

several collecting canals are one of the prominent structures.

The

endoplasm

is

more

fluid
it

and the ground substance

is

finely granu-

lated or reticulated;

undergoes rotation movement or cyclosis.

all euciliates.

Two
may
is

types of nuclei are present in

is

The massive

macronucleus
reach
space.

of various forms.

The chromatin
fill

granules which

20/x in

diameter

(p.

42)

compactly the intranuclear

amitosis.

The macronucleus

multiplies

by

The micronucleus

ordinarily so minute that

it is difficult

to see in a living specimen.

pact,

although in some it appears to be comand consists of an endosome, the chromatin, the nucleoplasm, and the membrane. The number of micronuclei present in an individual varies among different species. At the time of reproduction it increases in size and divides mitotically during conjugation it underIt is vesicular in structure,
;

goes a characteristic meiotic division

(p.

206).

from two to many nuclei of a uniformly same structure and numerous ovoid or spindle-shaped bodies, endospherules, the nature of which is open to speculation. Some authors
protociliates possess

The

think that they are nuclei (micronuclei (after Hickson, 1903) or macronuclei (after Konsuloff, 1922, 1930)); others consider them as
reserve food materials (Patten). Metcalf (1909) considers that each

nucleus possesses both metabolic chromatin and reproductive chromatin, the former being seen as large flattened peripheral masses and
the latter, as smaller spheroidal granules.

In

all

except protociliates and a comparatively small

number

of

CILIOPHORA, PROTOCILIATA
astomatous
is

685
its

euciliates, there is a

cytostome which in

simplest form

represented by a small opening on the pellicle, and may or may not be closed when the animal is not feeding. The cytostome opens into

the cytopharynx (or gullet), a tubule which ends in the deeper portion of the endoplasm. In the cytopharynx there may be present one
or

more undulating membranes

is

to facilitate intaking of the food.

surrounded by trichites or trichocysts (p. 71). When the cytostome is not at the anterior region as, for instance, in Paramecium, there is a peristome (or oral groove) which starts at or near the anterior end and runs posteriorly. The peristome is ciliated so that food particles are thrown down along it and ultimately into the cytostome which is located at its posterior end. Solid waste particles are extruded from the cytopyge, or cell-anus, which is usually noticeable only at the time of actual defecation (p. 108).
Occasionally the cytostome

Cytology (Konsuloff, 1922; Wetzel, 1925). Following Metcalf, Ciliata are here divided into 2 subclasses:

Two to many nuclei of one kind; sexual reproduction permanent fusion.

Subclass 1 Protociliata Macronucleus and micronucleus; sexual reproduction conjugation Subclass 2 Euciliata (p. 690)

Subclass

Protociliata Metcalf

The

protociliates are almost exclusively inhabitants of the large

intestine of Salientia; only a

few species have been reported from

urodeles, reptiles,

and

fish

(Metcalf, 1923, 1940).

The body

is

cov-

ered uniformly

by

cilia of

equal length. There

is

no cytostome and
of nuclei varies

the nutrition

is

parasitic (saprozoic).
all

The number

from two to many,

which are of one type. Asexual reproduction is by binary fission or plasmotomy. In a number of species sexual fusion of 2 gametes has been observed (Metcalf, 1909; Konsuloff, 1922) (Fig. 294, f-i). Grasse (1952) proposed recently to transfer these organisms to "Rhizoflagellata" from Ciliata, since they differ from the ciliates in (1) having nuclei of the same kind, (2) undergoing sexual fusion and not conjugation, and (3) having longitudinal, and not transverse, division or plasmotomy. Taxonomy (Metcalf,
of

1920a, 1923, 1940); geographical distribution (Metcalf, 1920, 1929, 1940); cytology and development (van Overbeek de Meyer, 1929);
species (Bhatia

and Gulati, 1927;

Carini, 1938-1942; Beltran, 1941,

1941a).

Family Opalinidae Claus

Genus Opalina Purkinje and Valentin. Highly

nucleate; in amphibians.

flattened; multi-

Numerous

species (Metcalf, 1923, 1940).

686

PROTOZOOLOGY
division (Hegner

Growth and nuclear

and Wu, 1921); cytology

(ten

Kate, 1927). 0. hylaxena Metcalf (Fig. 294,

a).

In Hyla versicolor; largerin divid28/z

ual about 420m

(Metcalf).
0. obtrigonoidea

long,

125m wide,

thick.

Several subspecies

M.

(Fig. 294, b-d). 400-840/x long, 175-180/x wide,

20-25ju thick; in various species of frogs

Bufo, Gastrophryne,
(Metcalf).

etc.),

and toads (Rana, Hyla, North America. Numerous subspecies

Fig. 294. a-i, 1, Metcalf; j, k, Leger and Duboscq. a, two individuals of Opalina hylaxena, X78; b-d, three individuals of 0. obtrigonoidea, X78 (b, from Bufo fowleri; c, from Rana pipiens; d, from R. palustris) e, four individuals of Cepedea cantabrigensis, X 78 f-i, stages in sexual reproduc; ;

tion in Protoopalina intestinalis;

j,

k,

P. saturnalis, X500;

1,

P. mitotica,

X240.

CILIOPHORA, PROTOCILIATA
0. carolinensisM. 90-400/x
cephala.

687

by 32-1 70/x;

in

Rana

pipiens spheno-

0. pickeringii

0. oregonensis 0. spiralis

M. 200-333m by 68-100/x; in Hyla pickeringii. M. 526m by 123m; in Hyla regilla. M. 300-355m long, 130-140m wide, 25-42m thick; M. About 470m by 100m; in Chorophilus M. About 240m by 85m; in Rana areolata.

in

Bufo compactilis.
0. chorophili
0. kennicotii
triseriatus.

cross-section; multinucleate; all in

Genus Cepedea Metcalf. Cylindrical or pyriform; circular in Amphibia. Numerous species.

C. cantabrigensis

Cytology (Fernandez, 1947).

M.

(Fig. 294, e).

About 350m by 84m;

in

in

Rana

cantabrigensis.

C.

hawaiensis

M. 170-200m by 43-60m;
98m; in Bufo

Rana

catesbeiana;

Hawaii.
C. obovoidea

M. About 315m by

Fig. 295. Zelleriella elliptica, stained specimens,

typical vegetative individual; b, an individual which

X440
is

(Chen), a, a nearly completely

divided, the nuclei being at early metaphase.

688

PROTOZOOLOGY
cir-

C. floridensis M. About 230m by 89m; in Scaphiopus albus. Genus Protoopalina Metcalf. Cylindrical or spindle-shaped,

cular in cross-section; 2 nuclei; in the colon of various species of

Amin

phibia with one exception.

Numerous

species.

P. intestinalis (Stein) (Fig. 294, f-i). About 330/x Bombina bombina, and B. pachypa; Europe. P. saturnalis Leger and
fish,

by 68m;

Box

boops; 100-152/x

P. mitotica (M) (Fig.

Duboscq (Fig. 294, j, k). In the marine by 22-60m294, 1). 300m by 37m; in Amby stoma tigrinum.

Genus
in

Zelleriella Metcalf. Greatly flattened; 2 similar nuclei; all

Amphibia. Numerous
Z. scaphiopodos

M.

species. Cytology (Chen, 1948). In Scaphiopus solitarius; about 150m long, 90m

broad, 13m thick.

Z. antilliensis (M).

About 180m

long, 113/z wide, 32/x thick; in

Bufo marinus.
Z. hirsuta
natus.

M. About

113m long, 60m wide, 22m thick; in Bufo cog-

Z. elliptica Chen (Fig. 295). In Bufo valliceps; average dimensions 184^ by 91m- Chen (1948) distinguishes four other species from the same host, all of which possess 24 chromosomes.

References

Butschli, O.: (1887-1889) Protozoa. In: Bronn's Klassen und

Ordnungen des Thier-reichs. 1. Doflein, F. and Reichenow, E. (1929) Lehrbuch der Protozoen:

kunde. 5 ed. Jena. Kahl, A.: (1930-1935) Urtiere oder Protozoa. I. Wimpertiere oder Ciliata (Infusoria). In: Dahl's Die Tierwelt Deutschlands und der angrenzenden Meeresteile, etc. Parts 18, 21, 25, 30. Kent, W. S. (1880-1882) A manual of Infusoria. London. Stein, F.: (1867) Der Organismus der Infusionsthiere. 2. Stokes, A. C: (1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71.
:

Beltran,

E.: (1941) Opalinidos parasitos en anfibios mexicanos.

Rev. Soc. Mexicana Hist. Nat., 2:127.

(1941a) Zelleriella leptodeirae sp. nov., etc. Ibid., 2:267.

Bhatia, B. L. and Gulati, A. N.: (1927) On some parasitic ciliates from Indian frogs, toads, etc. Arch. Protist., 57:85. Carini, A.: (1938) Contribuicao ao conhecimento das "Opalinidae" dos batraquios do Brasil. II. Bol. Biol, N.S., 3:147.

(1938a)

Zelleriella corniola, etc. Arch. Biol., 22:1. (1940) Contribuicao ao conhecimento das "Opalinidae" dos batraquios do Brasil. Ibid., 24, 5 pp. (1942) Sobre uma Zelleriella do cecum do Siphonops annulatus. Ibid., 26, 2 pp.

CILIOPHORA, PROTOCILIATA
Chen, T.

689

T.: (1948) Chromosomes in Opalinidae with special reference to their behavior, morphology, etc. J. Morphol., 88:281. Fernandez, D. F.-G.: (1947) Observaciones cytologicas sobre las Opalinas. Trab. Inst. Cien. Nat. Jose de Acosta, 1:352. Grasse, P.-P.: (1952) Traite de Zoologie. I. Fasc. 1. Paris. Hegner, R. W.: (1932) Observations and experiments on the opaJ. Parasitol., 18:274. linid ciliates of the green frog. and Wu, H. F.: (1921) An analysis of the relation between growth and nuclear division in a parasitic infusorian, Oplaina Am. Nat., 55:335. sp. Konsuloff, S.: (1922) Untersuchungen ueber Opalina Arch. Protist 44:285. (1930) Haben die Opaliniden zwei Kernarten wie die anderen Infusorien? Ibid., 71:248. Metcalf, M. M.: (1909) Opalina. Arch. Protist., 13:195. (1920) Upon an important method of studying problems of relationship and of geographical distribution. Proc. Nat. Acad. Sc, 6:432. (1920a) The classification of the Opalinidae. Science, 52:135. (1923) The opalinid ciliate infusorians. Smithsonian Inst. U. S.Nat. Mus., Bull., 120:1 (1928) The bell-toads and their opalinid parasites. Am. Nat.,

ten

van

62:5. (1929) Parasites and the aid they given in problems of taxonomy, geographical distribution and paleogeography. Smithsonian Misc. Coll., 81: no. 8. (1940) Further studies on the opalinid ciliate infusorians and Proc. U. S. Nat. Mus., 87:465. their hosts. Kate, C. G. B.: (1927) Ueber das Fibrillensystem der Ciliaten. Arch. Protist., 57:362. Overbeek de Meyer, G. A. W. (1929) Beitrage zur Wach:

stums- und Plasmadifferenzierungs-Erscheinungen an Opalina ranarum. Arch. Protist., 66:207. Wetzel, A.: (1925) Vergleichend cytologische Untersuchungen an
Ciliaten. Ibid., 51:209.

Chapter 31
Subclass 2 Euciliata Metcalf
most conspicuous group Protozoa containing 2 THE through macronucleus and micronucleus. Sexual reproduction
of
is

nuclei;

conjugation.
sive

We

owe Kahl a

great deal for his series of compreheneuciliates are

taxonomic studies of free-living ciliates. The grouped under the following four orders:
Without adoral zone of membranellae With adoral zone of membranellae

Order

Holotricha

Adoral zone winds clockwise to cytostome Peristome not extending beyond general body surface Order 2 Spirotricha Order 3 Chonotricha Peristome extending out like funnel. Adoral zone winds counter-clockwise to cytostome Order 4 Peritricha
. . .

(p.
(p.

796) 847)

(p.

850)

For a
reader

brief,

but concise view on the

classification of the ciliates, the

is

referred to Faure-Fremiet (1950).

Order

Holotricha Stein

The members
body

of this order

show uniform

ciliation

over the entire

possess a

surface. Adoral zone does not occur.

The majority

cytostome which varies among different forms. Nutrition is holozoic or saprozoic. Asexual reproduction is usually by transverse fission and sexual reproduction by conjugation. Encystment is common. The holotrichous ciliates are conspicuous free-living forms in all sorts of fresh, brackish, and salt waters, though some are parasitic.

The order is here

divided into 6 suborders:

Without cytostome Suborder 1 Astomata (p. 691) With cytostome Cytostome not rosette-like Without special thigmotactic ciliated field Cytostome on body surface or in peristome, without strong cilia
.

Suborder 2 Gymnostomata

(p.

700)

in peristome, bearing special cilia or membranes Peristome lined with rows of free cilia Suborder 3 Trichostomata (p. 737) Peristome with membrane; with or without free cilia Suborder 4 Hymenostomata (p. 758) With well-developed thigmotactic ciliated field; commensals in mussels Suborder 5 Thigmotricha (p. 774) Cytostome small rosette-like aperture or obscure; parasitic Suborder 6 Apostomea (p. 789)

Cytostome

EUCILIATA, HOLOTRICHA
Suborder
1

691

Astomata Schewiakoff

The
there

ciliates

placed in this suborder possess no cytostome, although

slit-like

may

occur a

organella which has been looked

ciliation is usually uniform.

upon

as

a vestigial cytostome.
division

The body

Asexual

is carried on by transverse fission and often by budding which results in chain formation. Sexual reproduction is conjugation and in some encystment is known. These organisms are parasitic

in various invertebrates living in fresh or salt water.

Taxonomy

(Cepede, 1910, 1923; Cheissin, 1930; Heidenreich, 1935; Delphy, 1936); skeletal structures (Rossolimo and Perzewa, 1929); Argyrome
(Puytorac, 1951).

Without attaching organellae or skeletal structures Macronucleus round to elongate Family 1 Anoplophryidae Macronucleus irregular network Family 2 Opalinopsidae (p. 694) With attaching organellae or skeletal structures
Contractile vacuole, a long dorsal ganella Contractile vacuoles not canal-like; or skeletal structures
canal; usually with a sucking or.

Family 3 Haptophryidae Family 4 Intoshellinidae

(p.

694) 696)

with various attaching organellae

(p.

Family

Anoplophryidae Cepede

(Collinia Cepede). Oval, elongate, macronucleus ovoid to cylindrical; micronucleus small; one to several contractile vacuoles; ciliation dense and uniform; in coelom and gut of Annelida and Crustacea. Numerellipsoid or cylindrical;

Genus Anoplophrya Stein

ous species (Rossolimo, 1926). A. marylandensis Conklin (Fig. 296,

intestine of

a).

36-72ju

by

16-42ju; in the

Lumbricus

terrestris

and Helodrilus caliginosus; Balti-

more, Maryland (Conklin, 1930). A. orchestii Summers and Kidder (Fig. 296, b). Polymorphic according to size; pyriform to broadly ovoid; 7-45 ciliary rows meridional, unequally spaced, and more on one surface; macronucleus voluminous, a compact micro nucleus; body 6-68/z long; in the sandflea, Orchestia agilis; Woods Hole, Massachusetts (Summers and Kidder, 1936). Genus Rhizocaryum Caullery and Mesnil. With hollowed ventral surface which serves for attachment; macronucleus drawn out like a
tree-root.

One

species.

R. concavum C. and

M.

(Fig. 296, c). In the

gut of Polydora caeca

and P. flava (polychaetes). Genus Metaphrya Ikeda. Pyriform, anterior end bent slightly to one side; 12 longitudinal ciliary furrows; below ectoplasm, a

692

PROTOZOOLOGY
with a spacious hollow; a micronucleus; no contractile
species.

layer of refringent materials; endoplasm sparse; macronucleus basket-like, large,

vacuoles.

One

M
for

sagittae I. (Fig. 296, d).

About

250/z

by

130/x; in

the body cavity

of Sagitta sp.

Genus Perezella Cepede. Ovoid; ventral surface concave, serves

attachment; macronucleus
ellipsoid;

contractile vacuole ter-

^^h

JH

orchestii,

a, Anoplophrya rnarylandensis, X500 (Conklin); b, A. X500 (Summers and Kidder); c, Rhizocaryum concavum, X670 (C6pede); d, Metaphrya sagittae, X120 (Ikeda); e, Perezella pelagica, X340 (Cepede); f, Dogielella sphaerii, X470 (Poljansky); g, D. minuta, X670 (Poljansky); h, D. Virginia, X670 (Kepner and Carroll); Orchi-

Fig.

296.

i,

lophrya stellarum, X870; opheliae, X350 (Cepede).

j,

Kofoidella eleutheriae,

X270;

k, Biitschliella

EUCILIATA, HOLOTRICHA

693

minal; longitudinally, uniformly, ciliated. A few species. P. pelagica C. (Fig. 296, e). In the coelom of copepods (Ascartia,
Clausia, Paracalanus)
;

about

48/z long.

Genus Dogielella Poljansky. Pyriform; longitudinal

cal or elliptical micro nucleus; in the

ciliary rows;

contractile vacuole terminal; macronucleus spherical, with a spheri-

parenchyma

of flat worms or

molluscs. 4 species (Poljansky, 1925).

D. sphaerii P. (Fig. 296,

/).

40-10(V by 25-54^:

in

Sphaerium

corneum. Conjugation (Poljansky, 1926). D. minuta P. (Fig. 296, g). 12-28^ by up to

leucops (Platyhelminthes).

20/z; in

Stenoslomum

D. Virginia (Kepner and Carroll) (Fig. 296, h). 40-50> long; in the same host animal; Virginia. D. renalis Kay. Elongate pyriform, but extremely plastic; 61-184^ by 27-82ju; spherical macronucleus in the middle of body; one micronucleus; a contractile vacuole anterior; in the renal organ of Phy sella
sp.

(Kay, 1946).
ciliary

Genus Orchitophrya Cepede. Elongate pyriform; oblique; macronucleus spherical, central. One species.

rows

0. stellarum C. (Fig. 296, i). In gonads of the echinoderm, Asteracanthion (Asterias) rubens; 35 65m long.

Genus Kofoidella Cepede. Pyriform; macronucleus broadly oval;

contractile vacuole, subterminal.

One

species.

K. eleutheriae C. (Fig. 296, j). In gastro vascular cavity of the medusa, Eleutheria dichotoma; 30-80/x long. Genus Herpetophrya Siedlecki. Ovoid; with a pointed, mobile, tactile, non-ciliated cone; macronucleus globular; without contractile vacuole.

One

species.

H. astomata S. In coelom of Polymnia (annelid). Genus Biitschliella Awerinzew. Elongate with pointed anterior end, with non-ciliated retractile anterior cap; cilia in about 10 slightly spiral rows; macronucleus band-form; several contractile
vacuoles in a longitudinal row. Several species. B. opheliae A. (Fig. 296, k). In Ophelia limacina; 280-360m by
35-50/x.

B. chaetogastri Penard. Elongate lanceolate, slightly flattened;

longitudinal rows of long
cilia;

cytoplasm

colorless;

macronucleus

elongate; micro nucleus voluminous, vesicular; without contractile

vacuole; 60-120/x long; in the oesophagus of Chaetogaster sp. Genus Spirobutschliella Hovasse (1950). Elongate fusiform with

rounded extremities;

ciliation

tip not ciliated; pellicle thick;

uniform and in spiral rows; anterior macronucleus, a long spindle reaching

694

PROTOZOOLOGY

the both ends of the body; a median micronucleus; in the intestine of

Annelida.
S. chattoni

H. In the mid-gut of Potamoceros

triqueter,

common

annelid in the vicinity of Banyuls; 180-550/x by 50/x; micronucleus

fusiform, 6-IOm long; often infected

by a microsporidian, Gurleya

nova H.

Genus Protanoplophrya Miyashita. Similar to Anoplophrya; but with rudimentary oral apparatus, a long slit, an undulating membrane and cytopharynx in anterior region of body; macronucleus elongate band numerous contractile vacuoles. One species. P. stomata Miyashita (Fig. 297, a). Cylindrical; up to 1.5 mm. by
;

about 70m;

in hind-gut of

Viviparus japonicus and V. malleatus.

Family 2 Opalinopsidae Hartog

Genus Opalinopsis Foettinger. Oval or fragmented; ciliation uniform and close;

cephalopods.
deletii

ellipsoid;

macronucleus

parasite in the liver of

few species.

0. sepiolae F. (Fig. 297, b). 40-80m long; in the liver of Sepiola ron-

and Octopus tetracirrhus. Genus Chromidina Gonder (Benedenia Foettinger). Elongate;

ciliation;

anterior region broader, end pointed; uniform

macro-

nucleus in irregular network distributed throughout body; micronucleus obscure; budding and encystment; Cheissin holds that this
is

identical with Opalinopsis.

One

species.

c, d). 500-1500m by about 30-60m kidney and gonad of cephalopods: Sepia, Loligo, Illex and Spirula (Jepps, 1931). Morphology (Wermel, 1928).

C. elegans (Foettinger) (Fig. 297,

in

Family 3 Haptophryidae Cepede

Stein. Elongate; uniformly ciliated; anterior end with a neck-like constriction; a circular sucker surrounded by 1-2 rows of cilia. A few species. H. michiganensis Wcodhead (Fig. 297, e). 1.1-1.6 mm. long; in the gut of the four-toed salamander, Hemidactylium scutatum; Michigan. Cytology (Bush, 1933); contractile canal (MacLennan, 1944). H. virginiensis Meyer. 354/x by 95m; macronucleus about one-

Genus Haptophrya

third of the

body length;

in the intestine of

Rana

palustris.

Genus

Steinella Cepede. Anterior end broad; sucker-like deprescilia,

sion without encircling

of Planaria ulvae,

but with 2 chitinous hooks. One

species.

S. uncinata (Schultze).

Up

to 200m long; in gastro vascular cavity at anterior

Gunda segmentata and Proceros sp. Genus Lachmannella Cepede. With a chitinous hook

EUCILIATA, HOLOTRICHA

695

end; elongate pyriform, anterior end curved; ciliation longitudinal

and dense. One

species.

L. recurva (Claparede

and Lachmann)

(Fig. 297, /).

In the gastro-

vascular cavity of Planaria limaeina; about 200/* long.

Genus
S.

Sieboldiellina Collin. Vermiform, with neck-like constric-

tion; simple sucker at anterior end.

One
g).

species.

planariarum (Siebold) (Fig. 297,

Up

to 70(V long; in gastro-

a, Protanoplophrya stomata, X100 (Miyashita); b, Opalinopsis X670 (Gonder); c, d, Chromidina elegans (c, X330 (Chatton and Lwoff); d, X220 (Wermel)); e, Haptophrya michiganensis, X35 (Woodhead) f, Lachmannella recurva, XlOO (C6pede) g, Sieboldiellina planariarum, X100 (Cepede);h, i, Intoshellina poljanskyi (h, X300; i, attaching

Fig. 297.

sepiolae,

organella seen from ventral side, X870) (Cheissin); j, k, Monodontophrya kijenskiji (j, XlOO; k, anterior end in profile, X870) (Cheissin).

696

PROTOZOOLOGY

vascular cavity of various fresh- and salt-water turbellarians, most

frequently Planaria torva.

Family 4 Intoshellinidae Cepede

ciliary rows slightly spiral; macronucleus voluminous, highly elongate; 5-7 contractile vacuoles scattered in posterior region; a complicated attaching organella at anterior end (Fig. 297, i) vestigial cytopharynx.
;

Genus Intoshellina Cepede. Elongate;

/.

poljanskyi Cheissin (Fig. 297,

h, i).

170-280/x long; in the intes-

tine of Limnodrilus arenarius.

Genus Monodontophrya Vejdowsky. Elongate; anterior end with

thick ectoplasm; attaching organella at anterior end, with fibrils;

macronucleus elongate; numerous contractile vacuoles in a longitudinal row.

M. kijenskiji Cheissin (Fig. 297, j, k). 400-800^ long; in anterior portion of intestine of Tubifex inflatus.
Genus Maupasella Cepede.
Ellipsoid; close longitudinal ciliary
fibrils;

rows; with a spinous attaching organella at anterior end, with

contractile vacuoles in 2 irregular rows; macronucleus elongate.

One species. M. nova C.

1920).

(Fig. 298, a).

70-130^ long;

in the intestine of Allolobo-

phora caliginosa (annelid). Supplementary chromatic body (Keilin,

Genus Schultzellina Cepede. Similar

to

Maupasella; but with at-

taching organella set obliquely; macronucleus voluminous, reniform. S. mucronata C. (Fig. 298, b). In the intestine of Allurus tetraedurus
(annelid).

Genus Hoplitophrya
tile

Stein. Slender, elongate; elongated

macro-

nucleus; a micronucleus; a single longitudinal row of

many

contrac-

vacuoles on the dorsal side; a single median spicule with a small

its

pointed tooth at
Several species.

anterior end; in the intestine of oligochaetes.

H. secansS. Elongated; 160-500/; by 20-35/x; 15-30 contractile

vacuoles in a row; spicule 10-15/x long; in the intestine of Lumbricus
variegatus.

H.

criodrili

Miyashita

(Fig. 298, c). Ellipsoid, slightly flattened;

90-130/x

by 45-60^; periphery

of

endoplasm highly granulated;

an

at-

taching organelle about 25/x long; macronucleus bandform; two rows

of contractile vacuoles; in the anterior half of the gut of
oligo-

chaete, Criodrilus sp.

Genus Radiophrya Rossolimo. Elongate, often with

satellites;

attaching organella composed of an arrowhead, a tooth and ecto-

EUCILIATA, HOLOTRICHA

697

Fig. 298.
nata,

a,

Maupasella nova, X280 (Cepede);

c,

b, Schultzellina

X670 (Cepede);

Hoplitophrya

criodrili,

X500

mucro(Miyashsita) d, e,
;

Radiophrya hoplites (Cheissin) (d, X 130; e, anterior end in profile, X300) f, Metradiophrya lumbrici, X140 (Cepede); g, Protoradiophrya fissispiculata,

X330 (Cheissin); h, Mrazekiella intermedia, Mesnilella rostrata, X470 (Cheissin); j, M. clavata,

X210 X290

(Cheissin);

i,

(Penard).

plasmic

fibrils;

macro nucleus a narrow long band; a

single

row

of

many

small contractile vacuoles, close to the nucleus.

Many

species.

R. hoplites R. (Fig. 298, d, e). 100-1000ju long; in the intestine of Lamprodrilus, Teleuscolex, Styloscolex, and other oligochaetes. Genus Metaradiophrya Heidenreich. Ovoid to ellipsoid; with 2
lateral

rows of contractile vacuoles; with a hook attached to a long

shaft; ectoplasmic fibers supporting the hook; in the intestine of

oligochaetes. Several species.

M.

intestine of

lumbrici (Dujardin) (Fig. 298,/). 120-140m by 60-70m; in the Lumbricus terrestris, L. rubellus and Eisenia foetida.
1951).

Morphology (Williams, 1942); argyrome (Puytorac,

698

PROTOZOOLOGY
by
by 55-70/x; hook 10/i long; shaft margin in ectoplasm; 25-30 support2 rows of 4 vacuoles each, which do not contract regularly
Beers. 115-150/x
2/x

M. asymmetrica
25-30/x

in antero -lateral

ing

fibrils;

in vitro; in the intestine (middle third) of Eisenia lonnbergi (Beers,

1938).

Genus Protoradiophrya Rossolimo. Elongate; near anterior end

a shallow depression along which
split posteriorly.
is

found a spicule which

g).

may

be

few species.
180-350/i long; in the ante-

P. fissispicidata Cheissin (Fig. 298,

rior portion of intestine of Styloscolex sp.

Genus Mrazekiella Kijenskij. Elongate; anterior portion broad with sucker-like depression, posterior region cylindrical; anterior end with attaching organella composed of arrowhead and skeletal
ribs;

tributed.

macronucleus an elongate band; contractile vacuoles A few species.

dis-

M.

intermedia Cheissin (Fig. 298, h). 180-260/* long; in the anterior

portion of intestine of Branchiura coccinea.

Genus Mesnilella Cepede. Elongate; with one or more long spicules imbedded in endoplasm; contractile vacuoles in 1-2 rows. Numerous
species.

M.

rostrata

Rossolimo

(Fig. 298,

i).

100-1200/x long; in the intes-

tine of various oligochaetes (Styloscolex, Teleuscolex, Lamprodrilus,

Agriodrilus, etc.).

M.

clavata (Leidy) (Fig. 298, j). 100-200/x long; in the intestine of

Lumbricus variegatus.
References

Beers, C. D.: (1938) Structure and division in the astomatous ciliJ. Elisha Mitch. Sc. ate Metaradiophrya asymmetrica n. sp. Soc, 54:111. Bush, Mildred: (1933) The morphology of the ciliate Haptophrya michiganensis, etc. Tr. Am. Micr. Soc, 52:223. Cepede, C.: (1910) Recherches sur les infusoires astomes: etc. Arch.
Bull. Soc. Zool. France, 48:105. (1923) V, VI. Cheissin, E.: (1930) Morphologische und systematische Studien ueber Astomata aus dem Baikalsee. Arch. Protist., 70:531. Conklin, C: (1930) Anoplophrya marylandensis, etc. Biol. Bull., 58:176. Delphy, Jean: (1936) Sur les Anoplophryimorphes. III. Bull. Mus. Nat. d'hist. nat., 8:516. Faure-Fremiet, E.: (1950) Morphologie compared et systematique des cilies. Bull. soc. zool. France, 75:109.

zool. exper. g6n., Ser. 5, 3:341.

Heidenreich, E.: (1935) Untersuchungen an parasitischen Ciliaten

aus Anneliden.
I, II.

Arch. Protist., 84:315.

EUCILIATA, HOLOTRICHA
Hovasse, R. (1950) Spirobutschliella Ocean ogr., no. 962.
:

699
etc.

chattoni,

Bull.

Inst.

Jepps,

Margaret W. (1931) On a parasitic ciliate from Spirula. Danish "Dana"-Exp. 1920-1922. Oceanogr. Rep., 8:35. Kay, Marie W. (1946) Observations on Dogielella renalis, etc. J.
: :

Parasitol., 32:197.

Keilin, D.: (1920) On the occurrence of a supplementary chromatic body in Mawpasclla nova, etc. Parasitology, 12:92. MacLennan, R. F.: (1944) The pulsatory cycle of the contractile canal in the ciliate Haptophrya. Tr. Am. Micr. Soc, 63: 187. Meyer, S. L.: (1939) Description of Haptophrya virginiensis, etc. J. Parasitol., 25:141. Miyashita, Y.: (1933) Drei neue parasitische Infusorien aus dem Darme einer japanischen Susswasseroligochaete. Ann. Zool.
Poljnskij,
Japon., 14:127. J. L: (1925)

Drei

dem Parenchym
Protist., 52:381.

einiger

neue parasitische Infusorien aus Mollusken und Turbellarien. Arch.

(1926) Die conjugation von Dogielella sphaerii. Ibid., 53: 407. Puytorac, P. de (1951) Sur le presence d'un argyrome chez quelques cilis astomes. Arch. zool. exper. gen., 88(N.-R) :49. Raabe, Z.: (1949) Recherches sur les cilies thigmotriches. IV. Ann. Univ. Maria Curie-Sklodowska, Sec. C, 4:195. Rossolimo, L. L.: (1926) Parasitische Infusorien aus dem Baikalsee.

Arch. Protist., 54:468. and Perzewa, T. A.: (1929) Zur Kenntnis einiger astomen Ibid., 67:237. Infusorien: etc. Summers, F. M. and Kidder, G. W.: (1936) Taxonomic and cytological studies on the ciliates associated with the amphipod family Ibid., 86:379. Orchestiidae from the Woods Hole district. Wermel, E. W.: (1928) Untersuchungen ueber Chormidina elegans. Ibid., 64:419. Williams, G. W. (1942) Observations on several species of Metaradiophrya. J. Morphol., 70:545. Woodhead, A. E.: (1928) Haptophrya michiganensis sp.nov. J. Parasitol., 14:177.
:

Chapter 32

Order

Holotricha Stein (continued)

Suborder 2 Gymnostomata Biitschli

Cytostome at or near anterior end Cytostome not at or near anterior end Cytostome lateral, narrow or round Cytostome ventral, in anterior half.
Tribe
Free-living
1

Tribe
. . .

Prostomata
(p.
(p.

Tribe 2 Pleurostomata .Tribe 3 Hypostomata

723) 728)

Prostomata Schewiakoff
trichites

Cytostomal region compressed; bearing

Family 1 Spathidiidae Cytostomal region not compressed Cytostome opens into anterior receptaculum with lorica Family 2 Metacystidae (p. 703) Cytostome at tip of apical cone Family 3 Didiniidae (p. 703) Cytostome otherwise
;

Body covered with

plates

regularly arranged, perforated, ectoplasmic Family 4 Colepidae (p. 706)

plates

Body not covered with

With

radially arranged tentacles

Without tentacles
Parasitic in

mammalian gut
Family
1

Family 5 Actinobolinidae Family 6 Holophryidae Family 7 Butschliidae

Spathidiidae Kahl

707) 708) (p. 717)

(p. (p.

Genus Spathidium Dujardin. Flask- or sack-shaped; compressed; anterior region slightly narrowed into a neck, and truncate; ciliation
uniform; cytostome occupies whole anterior end; contractile vacuole
posterior; macronucleus elongate; several micronuclei; trichocysts

around cytostome and scattered throughout; fresh or

salt water.

Numerous
water.

species.

S. spathula Miiller (Figs. 21, c; 299, a, b).

Up

to 250ju long; fresh

Morphology and food-capture (Woodruff and Spencer, 1922) conjugation (Woodruff and Spencer, 1924). Genus Paraspathidium Noland. Form resembles that of Spathidium; but cytostome an elongate slit, bordered on one side by strong cilia and on the other by weaker cilia and a shelf-like, nonundulatory membrane; 2 longer cilia on dorsal edge near anterior tip; anterior 1/3 compressed; posterior 2/3 nearly cylindrical; 2 oval macro nuclei, each with a micronucleus; cytoplasm filled with numerous refractile
granules; about 70 rows of
cilia;

contractile vacuole terminal; salt

water.

One

species.

44/x long each; salt water; Florida

P. trichostomum N. (Fig. 299, c-e). About 220/x long; macronuclei (Noland, 1937).
700

HOLOTRICHA

701

a, b, Spathidium spathula, X200 (Woodruff and Spencer); Paraspathidium trichostomum (Noland) (c, X130; d, cytostomal region X400; e, portion of pellicle, X1000); f, Spathidioides sulcata, X260 (Brodsky); g, Enchelydium fusidens, X240 (Kahl); h, Homalozoon vermiculare, X80 (Stokes); i, Cr another idiuni taeniatum, X300 (Schewiakoff) j, Penardiella crassa, X210 (Kahl); k, Perispria ovum, X665 (Dewey and Kidder); 1, P. strephosoma, X280 (Kahl); m, Legendrea bellerophon, X190

Fig. 299.

c-e,

(Penard).

Genus Spathidioides Brodsky

side

(Spathidiella

Kahl).

Somewhat

similar to Spathidium; but oral ridge highly flattened

side; this

and conspicuously developed into knob contains trichocysts; sapropelic.

on ventral a wart-like swelling on dorsal

end pointed,

S. sulcata B. (Fig. 299, /). 65-85/* long; posterior

702

PROTOZOOLOGY

highly flattened; anterior end elevated at one side where cytostome and cytopharynx with 10 rods are located.

Genus Enchelydium Kahl. Somewhat

similar to Spathidium; but

oral ridge forms a swollen ring with trichocysts; the ridge circular or

elongated in cross-section; when swimming, the organisms appear as if cytostome is opened; with dorsal bristle; fresh water. E. fusidens K. (Fig. 299, g). Cylindrical, contractile; cilia dense

and rather long; macronucleus reniform, often appears as composed

of 2 spherical parts; contractile vacuole terminal; oral ring with
spindle-like trichocysts; food vacuoles not seen; extended

body 110m

long; contracted 75m; sapropelic. Genus Homalozoon Stokes. Elongate; cilia conspicuous on flat-

tened right side;

left side

swollen or keeled; fresh water.

H. vermiculare (S.) (Fig. 299, h). Extended body 450-850m long; vermiform; macronucleus band form; contractile vacuoles about 30 or more in a row; standing fresh water. Genus Cranotheridium Schewiakoff. Spathidium-like organisms; anterior end obliquely truncate, near the extended side of which is located the cytostome; cytopharynx surrounded by a group of
trichites; fresh water.

C. taeniatum S. (Fig. 299,

i).

of trichites; macronucleus long band-form; with

Anterior end flattened; with a group many micro nuclei;

contractile vacuole terminal; ciliation

and

striation close; colorless;

movement

slow; about 170m long; fresh water.

Ellipsoid,

Genus Penardiella Kahl.

fresh water.

somewhat compressed;

oral

ridge slightly oblique; a girdle with trichocysts encircling the body;

P. crassa (Penard) (Fig. 299, j). Elongate ellipsoid, flattened; trichocysts in posterior portion of girdle are longer and those in the dorsal region are fewer in number and shorter; macronucleus sausage-form; contractile vacuole posterior, in front of the girdle; body

160m by 50m; sapropelic.

Genus Perispira
right-spirally

Stein.

Ovoid or

cylindrical;

oral

ridge turns

down

to posterior end.
k).

P. ovum S. (Fig. 299,

Oval; starved individuals 30-60m by 20-

45m, well-fed forms 65-120m by 50-1 10m; spiral ridge one complete turn; cytostome in the anterior end of the ridge, with a number of
delicate trichites; ovoid to elongate macronucleus; a micronucleus; a

terminal contractile vacuole; in fresh water

1940).

The

ciliate

was cultured

bacteria-free

(Dewey and Kidder, by feeding on sterile

about 85m

Euglena

gracilis.
/).

P. strephosoma Stokes (Fig. 299,

long; standing water with

Oval

to cylindrical;

sphagnum.

HOLOTRICHA

703

Genus Legendrea Faure-Fremiet. Ellipsoid or ovoid; a peripheral zone with small tentacular processes bearing trichocysts. L. bellerophon Penard (Fig. 299, m). 100-180/*; fresh water. Genus Teuthophrys Chatton and Beauchamp. Body rounded posteriorly,

anterior end with 3 radially equidistant, spirally curved

arms (counter-clockwise when viewed from posterior end); the depressions between arms form furrows; cytostome apical, at the inner
bases of arms; contractile vacuole terminal; ciliation uniform, except the inner surfaces of arms where longer
cysts are present; with
cilia as

well as tricho-

zoochlorellae; macronucleus rope-shaped

and wound; micro nucleus unobserved. One species. T. trisula C and B. (Fig. 300, a). 150-300/z long; length: width 3 1-2:1 ponds in Pennsylvania and California (Wenrich, 1929).
:
;

Family 2 Metacystidae Kahl

Genus Metacystis Cohn. Oblong;

rior

ciliation general, except poste-

end; ciliary circle around cytostome; usually one caudal cilium;

with a large posterior vesicle containing turbid fluid. M. truncata C. (Fig. 300, 6). Elongate, not much difference in body width at different levels; with about 12 furrow rings; body length up
to 30/x; salt water.

Genus Vasicola Tatem (Pelamphora Lauterborn). Ovoid with

caudal
end,
flask-shape, highly ringed; cytostome at anterior with 4 rows of long cilia; body surface with shorter cilia; macronucleus round, central, with a micro nucleus; contractile vacucilia; lorica

its lip

ole near macronucleus; fresh or salt water.

V. ciliata T. (Pelamphora butschlii L.) (Fig. 300,

c).

Body about

100m long; sapropelic in fresh water. Genus Pelatractus Kahl. Somewhat similar to Vasicola; but without lorica or caudal cilia; with a terminal vacuole; without lip of
Vasicola; sapropelic.

P. (Vasicola) grandis (Penard) (Fig. 300, d). Free-swimming; elongated fusiform; numerous contractile vacuoles on one side; body
125-220/x long; sapropelic in fresh water.

Family 3 Didiniidae Poche

Genus Didinium Stein (Monodinium Fabre-Domergue)

shaped; one to several girdles of
cilia (pectinellae)
;

Barrel-

expansible cyto-

stome at the tip of a proboscis, supported by a dense layer of long trichites; macronucleus horseshoe-shaped; two to three and occasionally four micronuclei, close to macronucleus; contractile vacuole terminal; fresh or salt water. Several species.

704

PROTOZOOLOGY

D. nasutum (Miiller) (Figs. 21, e, f; 40; 75; 91; 300, e-g). 80-200m endoplasm highly granulated; with two girdles of pectinelles; feeds on Paramecium spherical cysts (Fig. 75) with three walls, 6080 /x in diameter; fresh water. Morphology (Thon, 1905; Calkins, 1915; Beers, 1935); encystment, food requirement and conjugation
long;
;

(Beers, 1927, 1930, 1933, 1935); longevity of cysts (Beers, 1937);

a, Teuthophrys trisula, X330 (Wenrich); b, Metacystis trunX270 (Cohn); c, Vasicola ciliata, X250 (Kahl); d, Pelatr actus grandis, X170 (Penard); e-g, Didinium nasutum, X170 (Kudo); h, D. balbianii, X290 (Butschli) i-k, Mesodinium pulex (i, X670; j, oral view; k, oral tentacles, X1330) (Noland); 1, m, M. acarus (1, X670; m, oral tentacles, X1330) (Noland); n, Askenasia faurei, X530 (Faur^-Fremiet); o, Cyclotrichium meunieri, X780 (Powers).

Fig. 300.

cata,

HOLOTRICHA
excystment (Beers, 1945, 1946)
(Fig. 75); fibrillar structures

705
(ten

Kate, 1927); meiosis in conjugation (p. 206) (Prandtl, 1906). D. balbianii (Fab re-Do mergue) (Fig. 300, h). 60-100ju long; a single girdle of pectinelles near anterior end; fresh water. Genus Mesodinium Stein. Ovoid; an equatorial furrow marks
conical anterior

and spherical posterior parts;

in the

furrow are in-

serted 2 (or 1) rings of strong cilia; one directed anteriorly and the

other posteriorly; with tentacle-like retractile processes around the cytostome; fresh and salt water.
tacles

Lachmann) (Fig. 300, i-k). Oral tenwith trifurcate tips; body 20-3 1/x long; salt water; Florida. Noland states that the freshwater forms are 21-38^ long. M. acarus Stein (Fig. 300, I, m). Oral tentacles with capitate tip; 10-16m long; salt water, Florida (Noland, 1937).
pulex (Claparede and

M.

Fig. 301. Cyclotrichium meunieri (Bary and Stuckey). a, diagram of orin life, X665; b, a composite figure from stained specimens, X 1130 (c, cirri; ch, chromatophores; cr, ciliary row; cy, "cytostome"; py, pyrenoid).

ganism

Genus Askenasia Blochmann. Resembles Didinium; ovoid; with made up of some 60 pectinelles which are directed anteriorly; posterior ring composed of about the same number of long cilia directed posteriorly and arranged parallel to body surface; fresh or salt water. A. faurei Kahl (Fig. 300, n). Body oval, anterior end broadly
2 closely arranged rings of long cilia; anterior ring

second band

rounded; posterior region conical; pectinelles about 13/x long; the (10/z) of long cilia; an ellipsoid macronucleus; a micronucleus; body about 58-60^ long; fresh water. Genus Cyclotrichium Meunier. Body spheroid to ellipsoid with a large non-ciliated oral field which is surronded by a pectinelle-ring,

706

PROTOZOOLOGY

one end dome-like, and the other truncate; macronucleus sausageshaped; in salt water. C. meunieri Powers (Fig. 300, o; 301). Anterior end broadly rounded; posterior region conical; cytostome obscure; oral funnel at anterior end in a depression; broad filiated band at about middle; ectoplasm with concave chromatophore (covered with haematochrome) plates on surface, below which numerous pyrenoids occur in vacuoles; endoplasm with numerous granules; 25-42^ by 18-34^; Powers (1932) found that the 'red water' in Frenchman Bay in Maine was caused by the swarming of this organism. The same
author held later that this ciliate may be the same as Mesodinium rubrum as observed by Leegaard (1920). Bary and Stuckey (1950) found this organism in an extensive area of brownish-maroon water in Wellington Harbour in April and August, 1948. Their description follows: body 22-47/x by 19-41/z; anterior half dome-like, posterior half expanded; posterior end truncate; "cytostome"; greenish-maroon chromatophores close to body surface; no ingested food material.

Family 4 Colepidae Claparede and Lachmann

Genus Coleps Nitzsch. Body-form constant, barrel-shaped; with

regularly arranged ectoplasmic plates; cytostome at anterior end, surrounded by slightly longer cilia; often spinous projections at or near posterior end; 1 or more long caudal cilia, often overlooked; fresh or salt water. Many species (Noland, 1925, 1937; Kahl, 1930). C. hirtus (Miiller) (Fig. 302, a). 40-65/x long; 15-20 rows of platelets;

3 posterior processes; fresh water.

C. elongatus

Ehrenberg

(Fig. 302, b). 40-55ju long; slender;

about

13 rows (Noland, 1925) or 14-17 rows (Kahl) of platelets; 3 posterior

processes; fresh water.

C. bicuspis
lets;

Noland

(Fig. 302, c).

About 55m

long; 16 rows of plate-

2 posterior processes; fresh water. C. octospinus N. (Fig. 302, d). 80-1 10^ long; 8 posterior spines;

about 24 rows of platelets; Geiman (1931) found this organism in an acid marsh pond and noted variation in number and location of accessory spines; fresh water.
C. spiralis N. (Fig. 302,
e).

slightly spirally twisted; posterior spines

About 23 longitudinal rows of platelets drawn together; a long

water; Florida (Noland, 1937).

caudal cilium; about

50/z long; salt

C. heteracanthus N. (Fig. 302, /). Anterior processes only

side; posterior spines; caudal cilium;

on one
water;

about

90/x

by

35/x; salt

Florida.

HOLOTRICHA
Genus Tiarina Bergh. Somewhat
end tapering to a point; salt water. T.fusas (Claparede and Lachmann)

707

similar to Coleps, but posterior

(Fig. 302, g). 85-135/* long.

Family 5 Actinobolinidae Kent

Genus Actinobolina Strand (Actinobolus

cal; ciliation

Stein).

Ovate or spheri-

uniform; extensible tentacles among cilia; contractile vacuole terminal; macronucleus curved band; fresh water. A. vorax (Wenrich) (Fig. 302, h). Body 100-200/* long; elongate oval to spheroid; yellowish brown in color; cytostome at anterior end; contractile vacuole terminal; macronucleus rope-like; 30-60

Fig. 302. a, Coleps hirtus, X530 (Noland);b, C. elongatus, X530 (Noland); c, C. bicuspis, X530 (Noland); d, C. octospinus, X530 (Noland); e, C. spiralis, X400 (Noland); f, C. heter acanthus, X400 (Noland); g, Tiarina fusus, X530 (Faure-Fremiet) ; h, Actinobolina vorax, X300

(Wenrich);

i,

Dactylochlamys pisciformis, X330 (Kahl);

j,

Enchehjomor-

pha vermicularis, X670 (Kahl).

708

PROTOZOOLOGY

ciliary rows; about 30 tentacles in each ciliary row; tentacles may be extended to twice the diameter of the body or be completely withdrawn; feeds chiefly on rotifers which stop all movements as though completely paralyzed upon coming in contact with the tentacles

(Wenrich, 1929a).

Genus Dactylochlamys Lauterborn. Body spindle-form, though drawn out into tail; pellicle with 8-12 undulating spiral ridges on which tentacle-like processes and long cilia are alternately situated; these processes are retractile (Kahl) and
variable; posterior end
similar in structure to those of Suctoria; cytostome has not been

detected; possibly allied to Suctoria; fresh water.

One

species.

D. pisciformis L. (Fig. 302, i). Body 80-120/x long. Genus Enchelyomorpha Kahl. Conical, compressed; posterior end broadly rounded; anterior portion narrow; cilia on ring-furrows; anterior half with unretractile short tentacles; cytostome not noted; macro nucleus with a central endosome surrounded by spherules; contractile vacuole terminal, large.
E. vermicularis (Smith) (Fig. 302, j).
ish water.

Body 30-45/x

fresh

and brack-

Family 6 Holophryidae Schouteden

Genus Holophrya Ehrenberg. Oval, globose or

uniform; sometimes longer
cilia at

ellipsoidal; ciliation

the anterior or posterior region;

systostome circular, simple, without any ciliary ring around it; cytopharynx with or without trichites or trichocysts; fresh or salt
water.

Numerous
cilia

species.
(Fig. 304, a). Ellipsoidal;

H. simplex Schewiakoff
rows;

18-20 ciliary

uniformly long; cytostome small; cytopharynx without trichocysts or trichites; contractile vacuole and cytopyge posterior; macronucleus large, round; 34yu by 18/x; fresh water. Genus Lagynophrya Kahl. Resembles Holophrya; small elongate ovoid to short cylindrical; one side convex, the other more or less flattened; cytopharynx terminates anteriorly in a small cone-like process which may or may not be distinct; stagnant fresh or salt
water. Several species.
L. mutans K. (Fig. 304,
colorless;
b).

Body

plastic; oval to cylindrical;

narrowly striated; oval cone hemispherical without any trichocysts; body about 90ju long, when contracted about 65ju in diameter; among decaying leaves in fresh water. Genus Ichthyophthirius Fouquet. Body oval; ciliation uniform; pellicle longitudinally striated; cytostome at anterior end, with a short cytopharynx with cilia; horseshoe-shaped macronucleus;

HOLOTRICHA

709

micronucleus adhering to macronucleus; macronucleus undergoes reorganization by discarding small chromatin masses (Haas, 1934); no division within the host body; multiplication within cyst which is formed after dropping off the fish skin and in which numerous (up to

Fig. 303. Ichthyophthirius ?mdtijiliis. a, free-swimming individual, X75 development within cyst; f, a young individual, X400 (Fouquet); g, section through a fin of infected carp showing numerous parasites, XlO (Kudo); h, a catfish, Ameiurus albidus, heavily infected by
(Butschli); b-e,

the ciliate (Stiles, 1894).

1000) ciliated bodies (30-45^ in diameter) are produced; conjugation has been reported; parasitic in the integument of freshwater and marine fishes; in aquarium, host fish may suffer death; widely distributed.
/. multifiliis

F. (Fig. 303). 100-1000^ long; ovoid; produces pus-

tules in the epidermis or gills;

cytostome

is

large,

30-40^

in diameter.

710

PROTOZOOLOGY

Pearson (1932) and Kudo (1934) reported extensive infections in large open ponds in Indiana and Illinois and Butcher (1941, 1943) noted infections in many yearling trout in hatcheries in 1939 and 1940. MacLennan (1935, 1935a, 1937, 1942) observed that the grown trophozoites leave the host epithelium and encyst on the bottom of aquarium; the cytostome is absorbed; the body protoplasm divides into 100-1000 small spherical ciliated cells, 18-22^ in diameter, which presently metamorphose into elongated forms, measuring about 40^ to 10/x. These young ciliates break through the cyst wall

and seek new host

fish

by active swimming. The young

ciliates are

able to attack the fish integument for at least 96 hours, though their

markedly after 48 hours. Sikama (1938) observed a similar organism on 44 species of marine fishes. This ciliate was somewhat smaller in dimensions, measuring up to 452m by 360/z, and possessed a macronucleus typically
infectivity decreases

constricted into four beads. Fibrillar structures (ten Kate, 1927).

Genus Bursella Schmidt. Oval; anterior end broadly and obliquely truncate

where a large

ciliated groove-like pit occurs; ridges

of pit contractile; cilia short; macronucleus, spherical to ellipsoidal; several micronuclei; endoplasm reticulated; with symbiotic algae;

ectoplasm with trichocysts; fresh water. B. spumosa S. 240-560^ long; freshwater pond. Genus Spasmostoma Kahl. Somewhat similar to Holophrya; cytostome with flaps which beat alternately; ciliation uniform. S. viride K. (Fig. 304, c). Spherical or oval; always with green food vacuoles containing Euglena and allied flagellates; cytostome at anterior end; cytopharynx with trichocysts, which are extensible at the time when food is taken in; cilia on about 20 rows, near cytostome somewhat longer; macronucleus round; body 50-75^ long;
sapropelic.

Genus
Stokes).

Urotricha

Claraparede

and

Lachmann

(Balanitozoon

Body

caudal

cilia;

oval to ellipsoidal or conical; with 1 or more longer ciliation uniform, except in posterior region which may

be without

cilia;

cytostome at or near anterior end, surrounded by

ring of heavier cilia; contractile vacuole, posterior; macronucleus

spherical; fresh water.

swimming

U. agilis (Stokes) (Fig. 304, d). Body small; about 15-20m long; as well as leaping movement; standing fresh water with

sphagnum.
U. farcta C. and L. (Fig. 304, e). Body 20-30/x long; fresh water. Kahl considers U. parvula Penard and Balanitozoon gyrans Stokes
are identical with this species.

HOLOTRICHA

711

Fig. 304. a, Holophrya simplex, X800 (Roux); b, Lagynophrya mutans, (Kahl); c, Spasmostoma viride, X330 (Kahl); d, Urotricha agilis, (Stokes); e, U. far da, X470 (Lieberkiihn); f, g, Plagiocampa marina (Noland) (f, X400; g, anterior end, X670); h, Chilophrya utahensis,

X380 X530

X840 (Pack); i, C. labiata, X500 (Edmondson); j, Platyophrya lata, X280 (Kahl); k, Stephanopogon colpoda, non-ciliate side, X500 (Kahl); 1,
Prorodon discolor, X330 (Biitschli); m, Pseudoprorodon farctus, X270 (Roux); n, o, Coelosomides marina, X245 (Faure-Fremiet) (n, silver-impregnated surface view; o, optical section); p, q, Placus socialis, X530 (Noland) (p, anterior end view).

712

PROTOZOOLOGY

drical; slightly

Genus Plagiocampa Schewiakoff. Ovoid, spindle-form or cylinasymmetrical; cytostome at anterior end in a slit; right ridge thickened and lip-like, with about 8 long cilia; with or
salt water.

without long caudal cilium; fresh or

P. marina Kahl (Fig. 304,
salt
/, g).

Several species.

Cylindrical; oval macronucleus

;

central; contractile vacuole terminal; a caudal cilium 55-90/* long

water; Florida (Noland).

;

end, surrounded

Genus Chilophrya Kahl. Ovoid or ellipsoid cytostome at anterior by protrusible rods; on one side there is a lip-like
C. (Prorodon) utahensis (Pack) (Fig. 304, h).

ectoplasmic projection; fresh or salt water.

Body

ellipsoid,

somecilia-

what asymmetrical; comparatively small number

nucleus small,

of furrows;

tion uniform; a finger-like process in front of cytostome; macrocentral; contractile vacuole terminal; endoplasm with zoochlorellae; encystment common; cysts highly sensitive to light; 50m long; Great Salt Lake, Utah (Pack). C. (Urotricha) labiata (Edmondson) (Fig. 304, i). Body ovoid;

lip-like process in front of

cytostome; macronucleus oblong, central;

flask-like

contractile vacuole terminal; 30/* long; fresh water.

Genus Platyophrya Kahl. Compressed;

or elongate
flat

ovoid; asymmetrical; dorsal surface convex, ventral surface

or

partly concave; spiral striation; position and direction of cytostome

variable; macronucleus round; contractile vacuole terminal; fresh

water.
(Fig. 304, j). Highly compressed; colorless; many edge of cytostome 5-6 cirrus-like projections and on right edge many short bristles; 105/z long; fresh water with sphagnum. Genus Stephanopogon Entz. Somewhat resembles Platyophrya;

P.

lata

K.

striae;

on

left

compressed; cytostome at anterior extremity which is drawn out; cytostome surrounded by lobed membranous structures; salt water. S. colpoda E. (Fig. 304, k). Longitudinal striae on 'neck' 4-8 in

number; 2 contractile vacuoles; 50-70/* long; creeping movement;

salt

water among algae.

to

Genus Prorodon Ehrenberg (Rhagadostoma Kahl). Ovoid

cylindrical; ciliation uniform, with

sometimes longer caudal cilia; oral basket made up of double trichites which end deep in ectoplasm, oval in cross-section; contractile vacuole terminal; macronucleus
massive, spherical or oval; fresh or salt water.

Numerous

species.

P. discolor (E.) (Fig. 304, I). Ovoidal; 45-55 ciliary rows; macronucleus ellipsoid; micronucleus hemispherical; contractile vacuole terminal; 100-130/* long; fresh water; Kahl (1930) states that it occurs also in brackish water containing 2.5 per cent salt; sapropelic

HOLOTRICHA
form in
salt

713
cilia.

water

is

said to possess often long caudal

P. griseus Claparede and Lachmann. Oblong; 165-200/i long;

fresh water.

Genus Pseudoprorodon Blochmann. Similar

ously alveolated; trichocysts grouped;
1

to Prorodon; usually

flattened; one side convex, the other concave; ectoplasm conspicu-

or more contractile vacu-

oles posterior-lateral or distributed, with

many

pores; macronucleus

elongate; cytopharynx with trichites; fresh or salt water.

P. farctus (Claparede and Lachmann)

soid;

(Figs.

304,

m).

Ellip-

cytostome surrounded by long trichites; contractile vacuole posterior, with secondary vacuoles; macronucleus elongate; body
150-200/x long; fresh water.

Genus Coelosomides Anigstein (Coelosoma A.). General appearance similar to Prorodon and Holophrya; body cylindrical; ciliation uniform; at anterior end, a conspicuous ciliated vestibule runs down deep; mouth and cytopharynx; endoplasm vacuolated; a macronucleus and a micronucleus; marine.
C. marina A. (Fig. 304, n,
gate; micronucleus
o).

About

200/x long; central

endoplasm

highly vacuolated; periphery finely reticulated; macronucleus elon-

compact (Anigstein, 1911; Faure-Fremiet, 1950). Genus Placus Cohn (Spathidiopis Fabre-Domergue Thoracophrya Kahl). Body small; ellipsoid or ovoid; somewhat compressed;
;

with conspicuous spiral furrows; cytostome a narrow slit at slit; cytopyge a long narrow slit with cilia on both sides; macronucleus ellipsoid to sausage-form; contractile vacuole posterior; salt, brackish or
pellicle

anterior extremity; with strong cilia on right margin of

fresh water.

P. socialis (Fabre-Domergue) (Fig. 304, p, q). 40-50/* by 28-32/t, about 22^ thick; salt water; Florida (Noland, 1937). Genus Lacrymaria Ehrenberg. Polymorphic; cylindrical, spindleor flask-shaped; with a long contractile proboscis; cytostome round; ciliary rows meridional or spiral to right; near cytostome a ring-like constriction with a circle of longer cilia cytopharynx usually distinct; contractile vacuole terminal; fresh or salt water. Numerous
;

species.

L. olor (Miiller) (Fig. 305, a). Elongate; highly contractile; 2

macro nuclei; 2 contractile vacuoles; extended forms 400-500/* up to 1.2 mm. long; when dividing, long neck is formed sidewise so that it appears as oblique division (Penard) fresh and salt water. L. lagenula Claparede and Lachmann (Fig. 305, b). Body flaskshape; neck highly extensible; striation distinct, spiral when contracted; macronucleus short sausage-like or horseshoe-shape; endo;

714

PROTOZOOLOGY
;

plasm granulated; body 70m long, up to 150m (Kahl) salt water. L. coronata C. and L. (Fig. 305, c). Large; neck extensible; body form variable, but usually with bluntly rounded posterior end; endoplasm appears dark; striae spiral; 85-100/x long; salt and brackish
water.

Genus Enchelys
cate;

Hill.

cytostome

slit-like,

Flask-shape; anterior end obliquely trunrarely round; fresh or salt water. Several

species (Faur6-Fremiet, 1944).

E. curvilata (Smith) (Fig. 305, d). Elongate ovoid; posterior end rounded; longitudinal striation; macronucleus band-form; contractile vacuole terminal; endoplasm yellowish, granulated; about 150m long; fresh water among algae. Genus Crobylura Andre. Body when extended spindle-form, with truncate ends; when contracted, thimble-form; cilia short and thick; several long caudal cilia; slit-like cytostome at anterior end; no

apparent cytopharynx; macronucleus irregularly rounded, hard to stain; micro nucleus not observed; contractile vacuole latero-posterior; fresh water.

One

species.
e).

C. pelagica A. (Fig. 305,

Body 65-95m

long; in freshwater

plankton.
side convex; with a small slit-like cytostome near anterior end; with or without caudal bristle; fresh or salt water. M. {Enchelys) auduboni (Smith) (Fig. 305, /). Body plastic;

Genus Microregma Kahl. Small, ovoid; dorsal

flat;

ventral side

coarsely ciliated; caudal bristle thin; cytostome at anterior end,

surrounded by longer cilia; cytopharynx small with trichocysts; round macronucleus central; contractile vacuole near posterior end;

40-55m fresh water.

;

Genus Chaenea Quennerstedt. Elongate; anterior end drawn out into a narrow truncated 'head'; but without any ring furrow;
'head' spirally or longitudinally furrowed; often with longer cilia

directed anteriorly; cytostome terminal, not lateral; cytopharynx

with trichocysts; body striation meridional, or slightly right spiral; macronucleus often distributed; fresh or salt water. C. limicola Lauterborn (Fig. 305, g). Anterior half of body broad; posterior end drawn out into a point; contractile; cytopharynx with trichocysts; many trichocysts in endoplasm; contractile vacuoles in a row; 130-150m long; stagnant fresh water. Genus Pithothorax Kahl. Slender, barrel-shaped; with firm pellicle; a fairly long caudal bristle contractile vacuole in posterior half ciliation coarse and not over entire body surface; resembles Coleps; fresh
-

water.

HOLOTRICHA
P. ovatus K. (Fig. 305, h). Caudal bristle breaks off easily;
30/n long; fresh

715

body

water among decaying vegetation. Genus Rhopalophrya Kahl. Cylindrical; furrows widely separated; slightly asymmetrical; curved ventrally; dorsal surface convex; ventral surface flat or slightly concave; anterior end with 'neck'; 2
spherical macronuclei; fresh or salt water; sapropelic.

mSM.

.#!

v.v-'

..':-..--.v.,:C".i ..i"

Fig. 305. a, Lacrymaria olor, X170 (Roux); b, L. lagenula (contracted), (Calkins); c, L. coronata (contracted), X530 (Calkins); d, Enchelys curvilata, X200 (Smith); e, Crobylura pelagica, X500 (Andr6); f, Microregma auduboni X500 (Smith); g, Chaenea limicola, X310 (Penard); h, Pithothorax ovahis, X550 (Kahl); i, Trachelophyllum clavatum, X100 (Stokes).

X400

R. salina Kirby (Fig. 306, a). Cylindrical, tapering gradually to a truncated anterior end, slightly curved ventrally; cilia (6-10/* long)
sparsely distributed; 2 macronuclei, spherical; 29-55/z long; 16-21/x in diameter; in concentrated brine (salts "34.8 per cent; pH 9.48")

from Searles Lake; California (Kirby, 1934). Genus Enchelyodon Clapar&de and Lachmann. Elongated; cy-

716
lindrical,

PROTOZOOLOGY

ovoid or flask-shaped; some with head-like prolongation; cytopharynx with trichites; cilia long at anterior end; fresh or salt
water. Several species.

E. californicus Kahl. 120-130ju long; elongate ovoid to nearly

cylindrical; not distinctly flattened;

macro nucleus horseshoe-like,

flat-

with a large micronucleus; in mosses; California.

Genus Trachelophyllum Claparede and Lachmann. Elongate;

tened; flexible, ribbon-like; anterior end neck-like and tip truncate;

cytopharynx narrow, round in cross-section, with trichocysts; ciliary rows widely apart; 2 macro nuclei, each with a micronucleus; contractile

T. clavatum Stokes (Fig. 305,

vacuole terminal; fresh or salt water. Several species. i). About 200/x long; fresh water.

flask-shaped;

Genus Ileonema Stokes (Monomastix Roux). Body flattened; somewhat similar to Trachelophyllum, but there is a

remarkable flagellum-like process extending from anterior end; cytopharynx with trichocysts; fresh water. I. dispar S. (Fig. 306, 6). Highly contractile; anterior flagellum half body length, whose basal portion spirally furrowed; cytostome

Fig. 306. a, Rhopalophrya salina, X1040 (Kirby); b, Ileonema dispar, (Stokes); c, /. ciliata, X800 (Roux); d, e, Trachelocerca phaenicopterus (Kahl) (d, whole organism, X120; e, anterior end, X260); f, g, T, subviridis (Nolan d) (f, whole organism, XI 55; g, the nucleus, X480).

X190

HOLOTRICHA
at base of the flagellum;

717

cytopharynx spindle-form with trichites; 2 and cytopyge posterior; ovoid macronucleus; movement slow creeping; about 120/* long; fresh water among algae. I. ciliata (Roux) (Fig. 306, c). 75/* by 14/*; fresh water. Genus Trachelocerca Ehrenberg. Elongate, vermiform or flaskshaped; more or less extensible, with drawn-out anterior end; without any ring-furrow which marks the 'head' of Lacrymaria, and when contracted pellicular striae not spiral and no neck as is the case with
contractile vacuoles

Chaenea;

salt water.

Many
Cohn

species.
(Fig. 306, d, e). Elongate; extensible

and and tail distinct when contracted; cytostome at anterior end, surrounded by a ridge containing indistinctly visible short trichocysts, cytopharynx with trichocysts; macronuclei made up of 4 radially arranged endosomes suspended in the nucleoplasm
T. phoenicopterus
contractile; neck

(Gruber, Kahl); micronucleus difficult to make out; contractile vacuoles apparently in a row, rarely seen; salt water; Woods Hole
(Calkins).
T. subviridis Sauerbrey (Fig. 306,/, g).
tractile;

Highly extensible and con-

nucleus contains peculiar crystal-like bodies; size variable;

long; salt water.

when extended 320-480/*

Noland (1937) observed

the organism in a salt spring in Florida.

Family 7 Butschliidae Poche

This family includes species that inhabit the alimentary canal of

mammals;
fractile

circular

cytostome at anterior end, cytopyge usually

(Fig. 31, d) in anterior portion;

lo-

cated at posterior end; ciliation uniform or in a few zones; with re-

concrement vacuole

one or

more contractile vacuoles. Genus Butschlia Schuberg. Ovoid, anterior end truncate, posterior end rounded; cytostome at anterior end, surrounded by long cilia;
thick ectoplasm at anterior end; macronucleus spherical micronucleus(?); concretion vacuole; ciliation uniform; in

B. parva
1928).

S. (Fig. 307, a). 30-50/*

stomach of cattle. by 20-30/* Conjugation (Dogiel,

half con-

Genus Blepharoprosthium Bundle. Pyriform, anterior

tractile, ciliated;

caudal

cilia;

macronucleus reniform; in the caecum

and colon of horse. B. pirrum B. (Fig. 307, 6). 54-86/* by 34-52/* (Hsiung, 1930a). Genus Didesmis Fiorentini. Anterior end neck-like, with large cytostome; anterior and posterior ends ciliated; macronucleus ellipsoid; in the caecum and colon of horse. Species (Hsiung, 1930a).

718

PROTOZOOLOGY
c).

D. quadrata F. (Fig. 307,

groove.

50-90/z

by

33-68/*; with a deep dorsal

Genus Blepharosphaera Bundle. Spherical or ellipsoidal; ciliation uniform except in posterior region; caudal cilia; in the caecum and
colon of horse.

Fig. 307. a, Biltschlia parva, X670 (Schuberg); b, Blepharoprosthium pireum, X470 (Hsiung); c, Didesmis quadrata, X270 (Hsiung); d, Blepharosphaera intestinalis, X600 (Hsiung); e, Blepharoconus cervicalis, X360 (Hsiung); f, Bundleia postciliata, X530 (Hsiung); g, Blepharozoum zonatum, X200 (Gassovsky).

B. intestinalis B. (Fig. 307,

d).

38-74 M

in

diameter (Hsiung, 1930a).

Genus Blepharoconus Gassovsky. Oval; small cytostome; cilia on anterior 1/3-1/2; caudal cilia; macro nucleus ovoid; 3 contractile
vacuoles; cytopharynx with rods; in the colon of horse.

B. cervicalis Hsiung (Fig. 307,

1930, 1930a).

e).

56-83 m by 48-70m; Iowa (Hsiung,

Genus Bundleia da Cunha and Muniz. Ellipsoid; cytostome small; at anterior and posterior ends, posterior cilia much less numerous; in the caecum and colon of horse. B. postciliata (Bundle) (Fig. 307, /). 30-56m by 17-32 M (Hsiung,
cilia

1930a).

HOLOTRICHA
Genus Polymorphs Dogiel. Flask-shaped;
gion, a few caudal cilia;
ole terminal
;

719
ciliation

on anterior

re-

macronucleus disc-shaped; contractile vacu-

in

P. ampulla D. (Fig. 308,

the caecum and colon of horse. a). 22-36/* by 13-21 /* (Hsiung, 1930a).

Genus Holophryoides Gassovsky. Oval, with comparatively large cytostome at anterior end; ciliation uniform; macronucleus small,

b, Holophryoides Prorodonopsis coli, X700 (Gassovsky); d, Paraisotrichopsis composita, X450 (Hsiung); e, Sulcoarcus pellucidulus, X410 (Hsiung); f, Alloiozona trizona, X450 (Hsiung).

Fig. 308.

a,

Pohjmorpha ampulla, X1170 (Hsiung);

c,

ovalis,

X410 (Gassovsky);

ellipsoid; contractile vacuole subterminal; in the colon

and caecum

of horse.

H.

ovalis (Fiorentini) (Fig. 308, 6). 95-140/*

by

65-90/*.

Genus Blepharozoum Gassovsky.

terior end; ciliation uniform;
tractile vacuoles;

Ellipsoid, with attenuated pos-

cytostome near anterior tip; 2 conmacronucleus small, reniform; in caecum of horse.

g).

B. zonatum G. (Fig. 307,

1930a).

230-245/*

by 115-122/* (Hsiung,

720

PROTOZOOLOGY

contractile vacuoles;
horse.

Genus Prorodonopsis Gassovsky. Pyriform; ciliation uniform; 3 macro nucleus sausage-shaped; in the colon of

P. coli G. (Fig. 308, c). 55-67/* by 38-45/* (Hsiung, 1930a). Genus Paraisotrichopsis Gassovsky. Body uniformly ciliated; spiral groove from anterior to posterior end; in the caecum of horse. P. composite G. (Fig. 308, d). 43-56/* by 31-40/* (Hsiung, 1930a). Genus Sulcoarcus Hsiung. Ovoid, compressed a short spiral groove
;

at anterior end; cytostome at ventral

end of the groove; cytopyge

terminal; concretion vacuole mid- ventral, contractile vacuole posterior to it; cilia

on groove, posterior end and mid-ventral region

(Hsiung, 1935).
S. pellucidulus

H.

(Fig. 308, e). 33-56/*

by

30-40/*; in faeces of

mule.

Genus Alloiozona Hsiung. Cilia in 3 (anterior, equatorial and poscaecum and colon of horse (Hsiung, 1930, 1930a). A. trizona H. (Fig. 308,/). 50-90/* by 30-60/*. Genus Ampullacula Hsiung. Flask-shaped; posterior half bearing fine, short cilia; neck with longer cilia; in the caecum of horse. A. ampulla (Fiorentini). About 110/t by 40/* (Hsiung, 1930a).
terior) zones; in the

References

Anigstein, L.: (1911) Ueber zwei neue marine Ciliaten. Arch.

Protist., 24:127.

Bary, B. M. and Stuckey, R. G.: (1950) An occurrence in Wellington Harbour of Cyclotrichium meuvieri Powers, a ciliate causing red water, etc. Tr. Roy. Soc. New Zealand, 78:86. Beers, C. D.: (1927) Factors involved in encystment in the ciliate Didinium nasutum. J. Morphol. Physiol., 43:499.

On the possibility of indefinite reproduction in the Didinium, etc. Am. Nat., 63:125. (1933) Diet in relation to depression and recovery in the ciliate Didinium nasutum. Arch. Protist., 79:101. (1935) Structural changes during encystment and excystment. etc. Ibid., 84:133. (1945) The encystment process in the ciliate Didinium nasutum. J. Elisha Mitchell Sc. Soc, 61:264. (1946) Excystment in Didinium nasutum, with special reference to the role of bacteria. J. Exper. Zool., 103:201. Butcher, A. D. (1941) Outbreaks of white spot or ichthyophthiriasis (Ichthyophthirius multifiliis) at the hatcheries, etc. Proc. Roy.
(1930)
ciliate
:

Soc. Victoria, 53:126. (1943) Observations on some phases of the life cycle of Ichthyophthirius multifiliis, etc. Australian Zool., 10:125. Calkins, G. N.: (1915) Didinium nasutum. I. J. Exper. Zool., 19: 225.

HOLOTRICHA
Chatton, E. and Beauchamp,
:

721

P. D.: (1923) Teuthophrys trisulca, Arch. zool. exper. gen., 61 (N. et R.) 123. etc. Dewey, Virginia and Kidder, G. W.: (1940) Growth studies on
ciliates.

VI.

Biol. Bull., 79:255.

Dogiel, V.: (1928) Ueber die Conjugation von

Arch. Protist., 62:80.

Biitschlia parva.

Faure-Fremiet,

E.: (1944) Polymorphisme de YEnchelys rnutans. Bull. soc. zool. France, 69:212. (1950) Ecologie des cilies psammophiles littoraux. Bull. biol.

France Belgique, 84:35. J. and Ducornet, J.: (1948) Etude experi-, Stolkowski, mentale de la clacification tegumentaire chez un infusoire cilie" Coleps hirtus. Biochem. Biophys. Acta, 2:668. Geiman, Q. M.: (1931) Morphological variations in Coleps octospinus. Tr. Am. Micr. Soc, 50:136. Haas, G. (1934) Beitrage zur Kenntnis der Cytologic von Ich:

thyophthirius multifiliis. Arch. Protist., 82:88. Hsiung, T. S.: (1930) Some new ciliates from the large intestine of the horse. Tr. Am. Micr. Soc, 49:34. monograph on the Protozoa of the large intestine (1930a) of the horse. Iowa State College J. Sc, 4:356.

(1935)

On some new

ciliates

from the mule,

etc. Bull.

Fan

Mem.
:

Inst. Biol., 6:81.

Kahl, A. (1926) Neue und wenige bekannte Formen der holotrichen und heterotrichen Ciliaten. Arch. Protist., 55:197. (1927) Neue und erganzende Beobachtungen holotricher

Ciliaten.

I.

Ibid., 60:34.

(1930) Urtiere

oder

Protozoa.

I.

Dahl's

Die

Tierwelt

Deutschlands,

etc. Part. 18:1.

(1930a) Neue und erganzende Beobachtungen holotricher Arch. Protist., 70:313. Infusorien. II. Kirby, H. Jr.: (1934) Some ciliates from salt marshes in California.
Ibid., 82:114.

some protozoan parasites of fishes of Monogr., 13:1. Leegaard, C: (1920) Microplankton from the Finnish waters during the month of May, 1912. Acta Soc Sc. Fenn. Helsingfors,

Kudo, R. R.

(1934) Studies on

Illinois. Illinois Biol.

48:5:1.

MacLennan, R.

F.: (1935) Observations on the life cycle of Ichthyophthirius, etc. Northwest Sc, 9, 3 pp. (1935a) Dedifferentiation and redifferentiation in Ichthyophthirius. I. Arch. Protist., 86:191. (1937) Growth in the ciliate Ichthyophthirius. I. J. Exper. Zool, 76:423. (1942) II. Ibid., 91:1. Noland, L. E. (1925) review of the genus Coleps with descriptions of two new species. Tr. Am. Micr. Soc, 44:3. (1937) Observations on marine ciliates of the Gulf coast of Florida. Ibid., 56:160. Pearson, N. E.: (1932) Ichthyophthiriasis among the fishes of a pond in Indianapolis. Proc Indian Acad. Sc, 41:455.
:

722

PROTOZOOLOGY
E.: (1922) Etudes sur les infusoires d'eau douce. Geneva. P. B. A.: (1932) Cyclotrichium meunieri, etc. Biol. Bull., 63:

Penard, Powers,
74.

Prandtl, H.: (1906) Die Konjugation von Didiniumnasutum. Arch.

Protist., 7:251.
J. (1901) Faune infusorienne des eaux stagnantes de environs de Geneve. Mem. cour. fac. sc. l'Uni. Geneva, 148 pp. Sikama, Y. (1938) Ueber die Weisspunktchenkrankheit bei Seefischen. J. Shanghai Sc. Inst., 4:113. Stiles, C. W.: (1894) Report on a parasitic protozoan observed on fish in the aquarium. Bull. U. S. Fish Comm. for 1893, p. 173. Stokes, A. C.: C1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71, ten Kate, C. G. B.: (1927) Ueber das Fibrillensystem der Ciliaten. Arch. Protist., 57:362. Thon, K. (1905) Ueber den feineren Bau von Didinium, etc. Ibid.,

Roux,

5:281.

Wenrich, D. H.:

I.

(1929) Observations on some freshwater ciliates. Tr. Am. Micr. Soc, 48:221. (1929a) The structure and behavior of Actinobolus vorax.

Woodruff,

Biol. Bull, 56:390. L. L. and Spencer, H.: (1922) Studies spathula. I. J. Exper. Zool., 35:189.

on Spathidium

(1924) II.

Ibid.,

39:133.

Chapter 33

Order

Holotricha Stein (continued)

Suborder 2 Gymnostomata Biitschli (continued)

Tribe 2 Pleurostomata ScheAviakoff

Cytostome on convex ventral surface. Family 1 Amphileptidae Cytostome a long slit Cytostome round, at base of trichocyst-bearing neck Family 2 Tracheliidae (p. 725) Family 3 Loxodidae (p. 727) Cytostome on concave ventral side

Family

Amphileptidae Schouteden

Genus Amphileptus Ehrenberg. Flask-shaped; somewhat compressed; ciliation uniform and complete; slit-like cytostome not
tractile vacuoles; 2 or

reaching the middle of body, without trichocyst-borders; many conmore macro nuclei; fresh or salt water.

A. claparedei Stein (A. meleagris Claparede and Lachmann) (Fig. a). Slightly flattened; broadly flask-shaped; with bluntly pointed posterior and neck-like anterior end; cytostome about 2/5 from ventral margin; trichocysts indistinct; dorsal ciliary rows also
309,

not distinct; contractile vacuoles irregularly distributed; 120-150ju long; fresh and salt water, on stalks of Zoothamnium, Carchesium,
Epistylis, etc.

A. branchiarum Wenrich (Fig. 309,

of frog tadpoles;

b).

On the integument and

gills

swimming

individuals killed with iodine, 100-135/u

by 40-60/x (Wenrich, 1924). Genus Lionotus Wrzesniowski (Hemiophrys W.). Flask-shape; elongate, flattened; anterior region neck-like; cilia only on right side;
or

without trichocyst-borders; cytostome with trichocysts; 1 (terminal) many (in 1-2 rows) contractile vacuoles; 2 macronuclei; 1 micronucleus; fresh or salt water.
c). Elongate flask in form; hyawith flattened neck and tail, both of which are moderately contractile; posterior end bluntly rounded; without trichocysts; neck stout, bent toward the dorsal side; cytostome a long slit; contractile vacuole posterior; 2 spherical macronuclei between which a micronucleus is located; 100/i long; fresh water and probably also in

L. fasciola (Ehrenberg) (Fig. 309,

line;

salt water.

Genus Loxophyllum Dujardin (Opisthodon

lar to

Stein). Generally simi-

Lionotus in appearance; but ventral side with a hyaline border, reaching posterior end and bearing trichocysts; dorsal side with
723

724

PROTOZOOLOGY
macro nu-

either similar tricho cyst-border or with tricho cyst-warts;

cleus a single

mass
D.

or moniliform; contractile vacuole, one to

many;

fresh or salt water.

L. meleagris

Many

species.

(Fig. 309, d).

Form and

size highly variable;

seam with trichocysts and often undulating; dorsal seam narrow and near its edge, groups
flask-shape to broad leaf -like; broad ventral
of trichocysts in wart-like protuberances; macronucleus moniliform;

micronuclei, as
;

many

as the beads of the macronucleus (Penard,

;

1922) contractile vacuole terminal, with a long canal 300-400^ long,

up to

700ju (Penard); feeds

mainly on

rotifers; fresh water.

X370 (Roux); b, A. branchiarutn, X490 (Wenrich); c, Lionotus fasciola, X510 (Kahl); d, Loxophyllum meleagris, X120 (Penard); e, L. setigerum, X570 (Sauerbrey); f, Bryophyllum vorax, X360 (Stokes); g, h, Centrophorella fasciolatum (g, X50;h, XI 10) (Noland).
Fig. 309. a, Amphileptus claparedei,
flattened,

HOLOTRICHA
L. setigerum Quennerstedt (Fig. 309,
150/*
e).

725
100-350/* long; average

60m; form variable; 1-4 macro nuclei; several contractile vacuoles in a row; salt and brackish water. Morphology (Sauerbrey,

by

1928).

Genus Bryophyllum Kahl. Similar to Loxophyllum; but uniformly on both broad surfaces; ventral ridge with closely arranged trichocysts, extends to the posterior extremity and ends there or may continue on to the opposite side for some distance; macro nuciliated

cleus ovoid to coiled

bandform;

in mosses. Species (Gelei, 1933).

B. vorax (Stokes) (Fig. 309,/). Elongate; tricho cyst-bearing ventral ridge turns up a little on dorsal side; contractile vacuole pos-

macro nucleus oval; 130/* long; in fresh water among sphagnum. Genus Centrophorella Kahl ( Kentrophoros Sauerbrey). Extremely
terior;

elongate, nematode-like; anterior end greatly attenuated; posterior

end pointed; body surface longitudinally striated;

not observed.
C. fasciolalum (S.) (Fig. 309,
g, h).

ciliation

uniform;

1-3 macronuclei; numerous contractile vacuoles in 2 rows; cytostome

About
1

270+t

by

38/*.

Noland

(1937) observed 2 specimens in sediment taken from sandy bottom in

Florida; contracted 650/* long; extended

mm. long.

C. lanceolata Faure-Fremiet. Ribbon-like; 460-520/*

tral side ciliated; dorsal side

by 40 /*; vencovered with dark sulphur bacteria

flat of

(Caulobacteria), except the extremities; five to six spherical micronuclei,

about

4/* in

diameter; on sandy

Cape Cod (Faure-

Fremiet, 1951).

Family 2 Tracheliidae Kent

Genus Trachelius Schrank. Oval to spherical; anterior end drawn out into a relatively short finger-like process or a snout; posterior end rounded; round cytostome at base of neck; cyto pharynx with trichites; contractile vacuoles many; macro nucleus simple or bandform; fresh water.
flattened

ovum Ehrenberg (Fig. 310, a). Spheroidal to ellipsoid; right side and with a longitudinal groove; left side convex; proboscis about 1/4-1/2 the body length; cilia short and closely set; numerous
T.

contractile vacuoles; macronucleus short sausage-form, often di-

vided into spherules; endo plasm penetrated by branching cytoplasmic skeins or bands and often with numerous small brown excretion
granules; 200-400/* long; fresh water.
tion conspicuous;

Genus Dileptus Dujardin. Elongate; snout or neck-like prolongasomewhat bent dorsally; along convex ventral side

72g
of neck

PROTOZOOLOGY
many rows of trichocysts;
a row of strong
cilia;

dorsal surface

surrounded by a nng; cytoJiSr 3 rX end drawn out mto a tad, posterior nharynx with long trichocysts; ciliation umform; macronuvacuofes, 2 or more; body
of short bristles; cytostonre

ovum Xl30 Fig. 310. a, Trachehus (Hayes) d Z>. arwer, X310 c (Kahl); X250 (WeancbJ (Wenrich); e. P. ro6trft, X340

,7-

Y nn (Roux) CRouxV b ta
i,

'

X200 (Penard);
(Kahl);
i, j,

Loxodes Remanella rugosa

g,

,
(i,

J.
,

Dilevlus americanus, x340 coni

w|IIdri

Xl90

(S toke*

dorsal side,

n ? X13U, j, anienoi p

x8Q

(Kahl). ing the endoskeleton)

HOLOTRICHA
cleus bandform, moniliform or divided into

727

numerous independent

bodies; fresh or salt water.

Many

species.
b).

D. americanus Kahl (Fig. 310,

like;

Proboscis bent dorsally sickle-

macro nucleus made up of 2 sausage-shaped or often horseshoeshaped parts; 2 contractile vacuoles on dorsal side; 200/x long; in
mosses.

D. anser (Miiller) (Fig. 310,

c).

Proboscis slightly flattened; macro-

nucleus divided into 100 or more discoid bodies; 16 or more vesicular

micronuclei (Jones, 1951) contractile vacuoles in a row on the aboral
;

250-400 ju, sometimes up to 600/z long; encystment and excystment (Jones, 1951). Genus Paradileptus Wenrich (Tentaculifera Sokoloff). Body broader at the level of cytostome; with a wide peristomal field that bears the cytostome and is surrounded for 2/3-3/4 its circumference by a raised rim which is continuous anteriorly with the spirally wound proboscis; trichocyst-zone traversing the rim and anterior edge of proboscis; contractile vacuoles small, numerous, distributed; macronucleus segmented fresh water (Wenrich, 1929a).
surface, with 2-3 in proboscis;
in fresh water. Culture,
;

P. conicus
P.

W. (Fig. 310, d). 100-200m by 50-1 00/z. robustus W. (Fig. 310, e). 180-450/x long.

P. estensis Canella. 600-800^ long; feeds on rotifers (Canella,

1951).

Genus Branchioecetes Kahl. Preoral part somewhat like that of Amphileptus, and bent dorsally; ventral side of neck with 2 rows of trichocysts; cytostome at posterior end of neck; cytopharynx with
trichocysts; ectocommensals

on Asellus or Gammarus.

B. gammari (Penard) (Fig. 310,/). 130-200^ long; on

Gammarus.

Family 3 Loxodidae Butschli

Genus Loxodes Ehrenberg. Lancet-like; strongly compressed; anterior end curved ventrally, and usually pointed; right side slightly convex; uniform ciliation on about 12 longitudinal rows; ectoplasm
appears brownish, because of closely arranged brownish protrichocysts; endoplasm reticulated; 2 or more vesicular macro nuclei; one or

more micronuclei; 5-25

sal region; fresh water.

Miiller's vesicles (p. 87; Fig. 31, a, b) in dor-

L. vorax Stokes (Fig. 310, g). 125-140/z long; yellowish brown, a

row of slightly longer cilia; sapropelic in standing fresh water. L. magnus S. (Fig. 310, h). Extended about 700m long; dark brown; 12-20 or more Miiller's vesicles in a row along dorsal border; standing pond water. Genus Remanella Kahl. Similar to Loxodes in general appearance;

728

PROTOZOOLOGY

but with endoskeleton consisting of 12-20/x long spindle-form needles lying below broad ciliated surface in 3-5 longitudinal strings connected with fibrils; Muller's vesicles (Fig. 31, c) in some, said to be different from those of Loxodes (Kahl) sandy shore of sea. R. rugosa K. (Fig. 310, i, j). 200-300/x long.
;

Tribe 3 Hypostomata Schewiakoff

Without furrow;

pharyngeal basket on ventral surface Family 1 Nassulidae incomplete; Ciliation dorsal surface without cilia or with a few sensory
free-living; conspicuous oral or

Ciliation complete; dorsal cilia usually less dense than those

bristles

Posterior ventral surface with a style. .Family 2 Dysteriidae (p. 730) Without a style Family 3 Chlamydodontidae (p. 731) Furrow from anterior end of cytostome; parasitic

Family 4 Pycnothricidae

(p.

733)

Family

Nassulidae Schouteden
to elongate; ventral surface flat,

Genus Nassula Ehrenberg. Oval

dorsal surface convex; usually brightty colored, due to food material; cytostome 1/3-1/4 from anterior end; body often bent to left near cytostome; opening of oral basket deep, in a vestibule with a

membrane; macronucleus

spherical or ovoid, central; a single micro-

nucleus; contractile vacuole large, with accessory vacuoles and opens

ventrally through a tubule-pore; fresh or salt water.

Many species.

N. aurea E.
(Kahl).
sula;

(Fig. 311, a). 200-250/x long; fresh

and brackish water

Genus Paranassula Kahl. Similar in general appearance to Nasbut with preoral and dorsal suture line; longer caudal cilia on

dorsal suture; pharyngeal basket not funnel-like, with 16-18 trichites

about 75 ciliary rows; trichocysts especially in anterior region. P. microstoma (Claparede and Lachmann) (Fig. 311, b). Pellicle roughened by a criss-cross of longitudinal and circular furrows; macronucleus elongate oval, posterior; contractile vacuole near middle and right-dorsal; about 80-95/z long; salt water; Florida (Noland). Genus Cyclogramma Perty. Somewhat resembling Nassula; but conspicuous oral basket in pyriform depression and opens toward left on ventral surface; depression with a short row of small membranes at its anterior edge; trichocysts usually better developed than in
Nassula; fresh water.
C. trichocystis (Stokes) (Fig. 311,
c).

Body

colorless or slightly

rose-colored; trichocysts thick

and obliquely arranged; one confood vacuoles; actively

algae.

tractile vacuole; usually full of blue-green

motile; about 60/x long; in fresh water

among

HOLOTRICHA

729

stoma,

a, Nassula aurea, X190 (Schewiakoff); b, Paranassula microX400 (Noland); c, Cyclogramma trichocystis, X510 (Stokes); d, Chilodontopsis vorax, X200 (Stokes); e, Eucamptocerca longa, X320 (da Cunha); f, Orthodon hamatus, X160 (Entz); g, Dysteria calkinsi, X540 (Calkins); h, Trochilia palustris, X1070 (Roux); i, Trochilioides recta, X740 (Kahl); j, Hartmannula entzi, X220 (Entz); k, Chlamydodon mnemosyne, X520 (MacDougall); 1, Phascolodon vorticella, X340 (Stein).

Fig. 311.

Genus Chilodontopsis Blochmann. Elongate

ellipsoid; colorless;

ventral surface flattened, dorsal surface slightly convex; both sides

ciliated; oral basket without vestibule; cytostome with a membranous ring; usually with a postoral ciliary furrow; fresh water. C. vorax (Stokes) (Fig. 311, d). Elongate ellipsoid; anterior re-

730

PROTOZOOLOGY
left;

gion slightly curved to

snout fairly distinct; oral basket with

about 16 rods; several contractile vacuoles distributed, a large one terminal; macronucleus large, lenticular, granulated; with a closely attached micro nucleus 50-160/x long; fresh water. Genus Eucamptocerca da Cunha. Elongate; posterior part drawn out into a caudal prolongation dorso-ventrally flattened ciliation on both sides; round cytostome with oral basket in anterior ventral sur; ; ;

face.

One

species.

e). 300m by 25m; macronucleus ovoid, with a micro nucleus; contractile vacuole(?); in brackish water (salt con-

E. longa da C. (Fig. 311,

tent 3 per cent); Brazil.

Genus Orthodon Gruber. Oval;

and ventral

contractile; colorless;
left; striation

much

flat-

tened; anterior region curved toward

on both dorsal

sides; cytostome toward right border; oral basket long; macronucleus oval; contractile vacuole terminal; fresh or salt water. 0. hamatus G. (Fig. 311, /). Extended 200-260/x long, contracted 90-150/i long; flask-shaped oral basket with 16 trichites; salt water.
;

Family 2 Dysteriidae Kent

rede and

Genus Dysteria Huxley (Ervilia Dujardin; Iduna, Aegyria ClapaLachmann; Cypridium Kent). Ovate, dorsal surface conis

vex, ventral surface flat or concave; left ventral side with nonciliated

ventral plate; postoral ciliation

of cytostome

continuation of preoral to right

and

parallel to right margin;

cytostome in a furrow

near right side; posterior style or spine conspicuous; macronucleus spheroid or ovoid, central; with a micro nucleus; usually 2 contractile vacuoles; fresh or salt water. Numerous species.

D. calkinsi Kahl (Z). lanceolata Calkins) (Fig. 311, g). About 45m by 27m; salt water; Woods Hole. Genus Trochilia Dujardin. Similar to Dysteria; but ciliation on the ventral side in an arched zone; fresh or salt water. Several species.
T. palustris Stein (Fig. 311, A).

25m long; fresh water.

Genus Trochilioides Kahl. Rounded at anterior end, narrowed posteriorly; right side more convex than left; cytostome anterior with cytopharynx and preoral membrane; conspicuous longitudinal bands on right half with longitudinal striae, becoming shorter toward
left;

fresh or salt water.

T. recta
ish water.

K.

(Fig. 311,

i).

40-50m long; sapropelic

in fresh

and brack-

Genus Hartmannula Poche (Onychodactylus Entz). Ventral surface uniformly ciliated; cytopharynx with short rods; in salt water.
H.
entzi

Kahl

(Fig. 311, j).

80-140m long;

salt water.

HOLOTRICHA
Family 3 Chlamydodontidae Claus

731

Genus Chlamydodon Ehrenberg. Ellipsoid, reniform, elongate triangular, etc. cilia only on ventral surface, anterior cilia longer; cytostome elongate oval and covered with a membrane bearing a slit; oral basket made up of closely arranged rods with apical processes; along lateral margin, there is a characteristic striped band which is
;

a canalicule of
C.

unknown

function; fresh or salt water.

dorsal side greatly con-

mnemosyne E.
left side

(Fig. 311, k). Ellipsoid or reniform; right side

flat,

convex,
vex; a

concave; ventral side

band

of trichites, 'railroad track,' parallel to

body

outline; oral

basket with 8-10 rods; macro nucleus oval; 4-5 contractile vacuoles distributed; 60-90/x long; salt water. MacDougall (1928) observed it
in the brackish

water at Woods Hole and studied

Stein.
;

its

neuromotor

system.

Genus Phascolodon

Ovoid; with broad anterior end and

flat,

bluntly pointed posterior end ventral side concave or

dorsal side

convex; ciliated field on ventral surafce narrowed laterally behind cytostome, forming V-shaped ciliated area (about 12 rows); cytostome ellipsoid with oral basket; macronucleus oval with a micronucleus; 2 contractile vacuoles; fresh water.
P. vorticella S. (Fig. 311,
slit-bearing
l). 80-1 10m long; cytostome covered by a membrane; with 2 preoral membranes; macronucleus

ovoid; fresh water.

Genus Cryptopharynx Kahl.

ventral surface
flat,

Ellipsoid, anterior third bent to left;

dorsal surface with

hump;

spiral interciliary fur-

rows ridged; oval cytostome at anterior end; no cytopharynx; dorsal hump yellowish, granulated with gelatinous cover; 2 macro nuclei; 1 micro nucleus; 2 contractile vacuoles, one posterior and the other toward left side at the bend of body. One species. C. setigerus K. (Fig. 312, a, b). Elongate ellipsoid; anterior region bent to left; ventral surface flat, dorsal surface with a hump; about 15 ventral ciliary rows; 2 vesicular macronuclei and 1 micronucleus dorso-central; 33-96/x by 21-45m (Kirby). Kirby (1934) found the organism in salt marsh pools (salinity 1.2-9.7 per cent) with purple
bacteria; California.

Genus Chilodonella Strand (Chilodon Ehrenberg). Ovoid; dorsoventrally flattened; dorsal surface convex, ventral surface
tral surface
flat; venwith ciliary rows; anteriorly flattened dorsal surface with a cross-row of bristles; cytostome round; oral basket conspicuous, protrusible; macronucleus rounded; contractile vacuoles variable in number; fresh or salt water or ectocommensal on fish and amphi-

pods.

Many

species.

732

PROTOZOOLOGY
Blochmann)
(Figs. 53; 312,

C. cucullulus (Miiller) (Chilodon steini

c-e).

19-20 ventral ciliary rows; oral basket with about 12 rods and with 3 preoral membranes; macro nucleus oval, a characteristic concentric structure; micro nucleus small; body 100-300^ long, most

MHC;

Fig. 312. a, b, Cryptopharynx setigerus, X650 (Kirby); c-e, Chilodonella cucullulus (c, X270 (Stein); d, oral region; e, nucleus (Penard)); f, C. caudata, X1000 (Stokes); g, C. fiuviatilis, X800 (Stokes); h, C. cyprini,

X670 (Moroff);
mers).

i,

Allosphaerium palustris,

X1000 (Kidder and Sum-

often 130-150/x long; fresh and brackish water. Conjugation (Ivanic,

1933).
C. caudata (Stokes) (Fig. 312,/).

C. fiuviatilis (S.) (Fig. 312, g).

About 42/z long; standing water. About 50/i long; fresh water.

C. uncinata (Ehrenberg) (Fig. 96). 50-90/x long; about 11 ventral

HOLOTRICHA
ciliary

733

rows; some 7 dorsal bristles; widely distributed in various

several
varieties.

freshwater bodies;
1935).

Conjugation

(MacDougall,

by 3O-40m; in the integuorganism, if freed from the host body, dies in 12-24 hours. Ciliation (Krascheninnikow, 1934). C. longipharynx Kidder and Summers. 17-21/1 (average 19m) long;
C. cyprini (Moroff) (Fig. 312, h). 50-70m
fishes; the

ment and gills of cyprinoid

cytopharynx long, reaches posterior end; ectocommensal on amphipods, Talorchestia longicornis and Orchestia palustris; Woods Hole (Kidder and Summers, 1935). C. hyalina K. and S. 40ju (36-47m) long; ectocommensal on Orchestia agilis;

Woods
K. and

Hole.
S.

C. rotunda
chestia agilis;

29m (27-34/z) long; ectocommensal on Or-

Woods

Hole.

cave, left side

Genus Allosphaerium Kidder and Summers. Oval; right side conmore or less flat; body highly flattened; arched dorsal
rows; right and

surface devoid of cilia; ventral surface slightly concave with 12-27

ciliary
lar fold;
left margin of ventral surface with a pellicucytostome anterior-ventral, oval or irregular, surrounded by ridge on posterior border, extending to left margin; 3 groups of ciliary membranes extending out of cytostome; macro nucleus oval, central or anterior; a micro nucleus; 2 (or 1) contractile vacuoles; a

refractile spherule regularly present in posterior portion of endoplasm; ectocommensal on the carapace and gills of amphipods. A. palustris K. and S. (Fig. 312, i). 46-59/x long; 27 ventral ciliary rows; on Orchestia palustris and Talorchestia longicornis) Woods

Hole.
of Orchestia agilis
S. 24-32m long; 12 ciliary rows; on the carapace and 0. palustris; Woods Hole. A. granulosum K. and S. 32-42yu long; rotund; 17 ciliary rows; cytoplasm granulated; on carapace of Orchestia agilis and 0. palus-

A. sulcatum K. and

Woods Hole. A. caudatum K. and S. Resembles A. palustris; 35-45ju long; 14 ciliary rows; 1 contractile vacuole; ectoplasm at posterior end, drawn
tris;

out into a shelf; on Orchestia agilis; Woods Hole. A. convexa K. and S. 24-36m long; 17 ciliary rows; on the carapace

and

gill

lamellae of Talorchestia longicornis;

Woods

Hole.

Family 4 Pycnothricidae Poche

and conspicuous; a furrow or groove connects the cytostome with the anterior end; parasitic in the alimentary canal of mammals.
Ciliation uniform; ectoplasm thick

734

PROTOZOOLOGY

Genus Pycnothrix Schubotz. Large, elongate; with broadly rounded anterior and narrowed posterior end; somewhat flattened; short thick cilia throughout; ectoplasm thick; macro nucleus spherical, in anterior 1/6; micronucleus(?); 2 longitudinal grooves, one beginning on each side near anterior end, united at the notched posterior end; a series of apertures in grooves considered as cytostomes;

at posterior 1/3, an aperture gives rise to branching canals running

through endoplasm, and

species.

is

considered as excretory in function.

a).

One

P. monocystoides S. (Fig. 313,

Procavia capensis and P. brucei.

300ju-2

mm.

long; in the colon of

Genus

Nicollella

Chatton and Perard. Elongate; a narrow groove

extends from the anterior end to cytostome, located at the middle of

Fig. 313.

X170;
cata,

c,

Collinella gundi,

X395

Pycnothrix monocystoides, X50; b, Nicollella ctenodactyli, X170 (Chatton and P6rard); d, Buxtonella sul(Jameson); e, Taliaferria clarki, X500 (Hegner and Rees).
a,

HOLOTRICHA

735

body; bilobed posteriorly; contractile vacuole terminal; macronucleus ellipsoid, anterior; a micronucleus; ectoplasm thick anteriorly; ciliation uniform (Chatton and Perard, 1921). One species.

N.

ctenodactyli C.

and

P. (Fig. 313, b). 70-550/z

by 40-150/x;

in the

colon of Ctenodactylus gundi.

Collinella Chatton and Perard. More elongate than Nicoluniform ciliation; a groove extends from end to end; cytostome at posterior end of the groove; contractile vacuole terminal; macronucleus much elongated, central or posterior (Chatton and Perard,

Genus

lella;

1921).

One

species.

C. gundi C.

and P.

(Fig. 313, c).

550-600 m by 100m;

in the colon of

Ctenodactylus gundi.

Genus Buxtonella Jameson. Ovoid; a prominent curved groove bordered by two ridges from end to end; cytostome near anterior end; uniform ciliation; in the caecum of cattle (Jameson, 1926). One
species.

313, d). 55-124/x by 40-72 M Hegner and Rees. Body ovate; circular in crosssection; ectoplasm is two-layered and thick; ciliation uniform; cytostome anterior, subterminal; macronucleus and a closely attached micronucleus near center; two contractile vacuoles; cytopyge (Hegner and Rees, 1933). One species. T. clarki H. and R. (Fig. 313, e). 83-146/x by 42-83/z; in the caecum and colon of the red spider monkey (Ateles geoffroyi).

B. sulcata

J. (Fig.

Genus

Taliaferria

References

Chatton, E. and Perard, C: (1921) Les

Nicollelidae, infusoires

intestinaux des gondis et des damans, etc. Bull. biol. France et Belgique, 55: 87. Canella, M. F.: (1951) Contributi alia conoscenza dei Ciliati. II. Ann. Univ. Ferrara, Sez. 3, Biol. Anim., 1:81. da Cunha, A. M.: (1914) Beitrag zur Kenntnis der Protozoenfauna Brasiliens. Mem. Inst. Oswaldo Cruz, 6: 169. Faure-Fremiet, E.: (1951) The marine sand-dwelling ciliates of Cape Cod. Biol. Bull., 100:59. Gelei, J. v.: (1933) Beitrage zur Ciliatenfauna der Umgebung von Szeged. II. Arch. Protist., 81:201. Hegner, R. W. and Rees, C. W.: (1933) Taliaferria clarki, etc. Tr. Am. Micr. Soc, 52:317. Ivanic, M.: (1933) Die Conjugation von Chilodon cucullulus. Arch. Protist., 79:313. Jameson, A. P.: (1926) ciliate, Buxtonella sulcata, etc. Parasitology, 18:182. Jones, E. E. Jr.: (1951) Encystment, excystment, and the nuclear cycle in the ciliate Dileptus anser. J. El. Mitch. Sc. Soc, 67: 205.

736

PROTOZOOLOGY
Deutschlands,
etc. Part. 21.

Kahl, A.: (1931) Urtiere oder Protozoa. Dahl's Die Tierwelt Kent, W. S.: (1880-1882) A manual of Infusoria. Kidder, G. W. and Summers, F. M.: (1935) Taxonomic and etiological studies on the ciliates associated with the amphipod family, etc. I.

Biol. Bull, 68:51.

ciliates

Kirby, H. Jr.: (1934) Some

Arch. Protist., 82:114.

from

salt

marshes

in California.

Krascheninnikow,

S.: (1934) Ueber die Cilienanordnung bei Chilodonella cyprini, etc. Ann. Protist., 4:135. MacDougall, Mary S.: (1935) Cytological studies of the genus Chilodonella, etc. I. Arch. Protist., 84:198. Noland, L. E.: (1937) Observations on marine ciliates of the Gulf coast of Florida. Tr. Am. Micr. Soc, 56:160. Penard, E.: (1922) Etudes sur les infusoires d'eau douce. Geneva. Sauerbrey, Ernestine: (1928) Beobachtungen liber einige neue

oder wenig bekannte marine Ciliaten. Arch. Protist., 62:355. Stein, F.: (1867) Der Organismus der Infusionstiere. Vol. 2. Stokes, A. C: (1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71. Wenrich, D. H.: (1924) A new protozoan parasite, Amphileptus branchiarum, etc. Tr. Am. Micr. Soc, 63:191. Ibid., (1929) Observations on some freshwater ciliates. II. 48:352.

Chapter 34

Order

Holotricha Stein (continued)

With gelatinous

lorica;

Suborder 3 Trichostomata Biitschli swimming backward Family 1 Marynidae

(p.

738)

Without lorica Compressed, armor-like pellicle; ciliation sparse, mainly on flat right side in 2-9 broken rows on semicircular or crescentic keel; cytostome on flattened ventral surface, with an obscure membrane. Family 2 Trichopelmidae (p. 739) Body form and ciliation otherwise With a long caudal cilium; cilia in 3-4 spiral rows on anterior half, very small forms Family 3 Trimyemidae (p. 739) Without a caudal cilium; form and ciliation otherwise With a spiral zone of special cilia, from cytostome to posterior end Spiral zone extends from anterior right to posterior left Family 4 Spirozonidae (p. 740) Spiral zone extends from anterior left to posterior right Family 5 Trichospiridae (p. 740) Without a spiral zone of special cilia Ciliated cross-furrow in anterior 1/5 on ventral surface, leads Family 6 Plagiopylidae (p. 740) to cytostome Without ciliated cross-furrow Cytostome in flat oval groove with heavily ciliated ridge in anterior 1/4 Family 7 Clathrostomidae (p. 742)
Cj'tostome funnel-like, deeply situated Cytostomal funnel with strong cilia; peristome from anterior left to posterior right

Family 8 Parameciidae

(p.

742)

Without such a peristome

Free-living; oral funnel deep; cilia at

bottom and top. Family 9 Colpodidae (p. 745)

.

Endozoic

Commensal

in vertebrates

Family 10 Entorhipidiidae (p.748

Parasitic in vertebrates Ciliation uniform

With concrement vacuoles

Family 11 Paraisotrichidae Without such vacuoles Family 12 Isotrichidae
Ciliation not uniform
(p.

750)
751)

(p.

Cytostome occupies the

entire anterior end; cilia only in anterior region Family 13 Cyathodiniidae (p. 752) Cytostome not terminal; tufts of cilia above and below cytostome and in posterior region. Family 14 Blepharocoridae (p. 752)
.

737

738

PROTOZOOLOGY
infraciliature, but cilia only in free-swimming stage; adult enclosed within a thick pellicle and attached to secretory hair of arthropods Family 15 Conidophryidae (p. 753).

Body with

Family

Marynidae Poche

Genus Maryna Gruber. Peristome makes a complete circle, thus the cone is entirely separated from anterior edge of body; cytostome
left ventral,

elongate

slit;

ridge also with a

slit;

gelatinous lorica

dichotomous.

M.

socialis

G. (Fig. 314,

a, b).

About 150m

long; in infusion

made

from long-dried mud.

Fig. 314.
e, f,

a, b,

thrix erlangeri,

Maryna socialis (a, X40; b, X160) (Gruber); c, MycteroX310 (Kahl); d, Trichopelma sphagnetorum, X570 (Kahl);

dentata,
k,

Pseudomicrothorax agilis (e, X340; f, X670) (Kahl); g, Drepanomonas X540 (Penard); h, Microthorax simulans, X620 (Kahl); i, Trimyema compressum, X410 (Lackey); j, Spirozona caudata, X370 (Kahl);
Trichospira inversa,

X360

(Kahl).

HOLOTRICHA

739

Genus Mycterothrix Lauterborn (Trichorhynchus Balbiani). Anterior cone continuous on dorsal side with body ridge; hence free edge of body only on ventral side; no ventral slit.

M.

erlangeri L. (Fig. 314, c).

Nearly spherical with zoochlorellae;

50-55ju

by 40-50^;

fresh water.

Family 2 Trichopelmidae Kahl

Genus Trichopelma Levander (Leptopharynx Mermod). Compressed; surface with longitudinal furrows, seen as lines in end-view;

coarse ciliation throughout; cytostome toward left edge about 1/3

from the anterior end; cytopharynx tubular; macro nucleus spheroid,

central; 2 contractile vacuoles; fresh water.
T. sphagnetorum (L.) (Fig. 314, d).

25-40/x long; in fresh water.

Genus Pseudomicrothorax Mermod (Craspedothorax Sondheim).

More

or less compressed; cytostome opens in anterior half toward

left side, in

marked with a broad longitudinal

canal-like; cilia
;

a depression surrounded by ciliary rows; body surface ridge with cross striation; furrows

on ventral

side;

cytopharynx tubular, with

;

elastic

rods fresh water.

P. agilis

M.

(Fig. 314, e,f). Ellipsoid

48-58ju long; in fresh water.

Stein).

Genus Drepanomonas Fresenius (Drepanoceras

tened; aboral surface convex; oral surface
flat

Highly

flat-

or concave; with a few

deep longitudinal furrows; ciliation sparse; cytostome and a small cytopharynx simple, near the middle of body; fresh water. Several
species.

D. dentata F.

(Fig. 314, g).

2 rows of ciliary furrows

With a small process near cytostome; on both oral and aboral surfaces; cilia on

both ends of oral surface; 40-65/z long; in fresh water. Genus Microthorax Engelmann (Kreyella Kahl). Small, flattened; with delicate keeled armor which is more or less pointed anteriorly and rounded posteriorly; ventral armor with 3 ciliary rows; oral depression posterior-ventral, with a stiff ectoplasmic lip on right side, below which there is a small membrane, and with a small tooth on left margin; no cytopharynx; macro nucleus spherical; 2 contractile
vacuoles; in fresh water.

Many species.
h).

simulans Kahl (Fig. 314, sion, also in moss.

M.

30-35ju long; decaying plant infu-

Family 3 Trimyemidae Kahl

Genus Trimyema Lackey (Sciadostoma Kahl). Ovoid, more or

flattened; anterior

less

end bluntly pointed, posterior end similar or rounded; with a long caudal cilium; cilia on 3-4 spiral rows which are

740

PROTOZOOLOGY

usually located in the anterior half of body; round cytostome near

macro nucleus cenwith a small micronucleus; one contractile vacuole; active swimmer; fresh or salt water.
tral

anterior end with a small cytopharynx; spherical

compressum L. (Fig. 314, i). About 65/i by 35/t; Lackey found it Imhoff tank; fresh and salt water (Kahl). Klein (1930) studied its silverline system.
T.
in

Family 4 Spirozonidae Kahl

Genus Spirozona Kahl. Short spindle-form; anterior end truncate, posterior region drawn out to a rounded end, with a group of longer
cilia; spiral ciliation;

ciliary

row runs over ridge

beginning near right posterior third the central to left and then reaches the cytostome;

other rows are parallel to

it; cytostome in anterior 1/4, with cytopharynx; ellipsoid macro nucleus nearly central; contractile vacuole

terminal; fresh water, sapropelic.

S. caudata

K.

(Fig. 314, j).

80-100/* long.

Family 5 Trichospiridae Kahl

Genus Trichospira Roux. Body

spiral

cylindrical; posterior

end rounded,

anterior end conical in profile, where the cytostome surrounded

by 2

rows of cilia, is located; a special ciliary band beginning in the cytostomal region runs down on ventral side, turns spirally to left and circles partially posterior region of body; ciliary rows parallel to it; macro nucleus oval, with a micronucleus; contractile vacuole posterior; fresh water, sapropelic.

T. inversa (Claparede

and Lachmann)

(Fig. 314, k).

70-100/z long.

Family 6 Plagiopylidae Schewiakoff

Genus Plagiopyla Stein. Peristome a broad ventrally opened groove from which body ciliation begins; peristomal cilia short, except a zone of longer cilia at anterior end; cytostome near median line at the
end of the peristome; cytopharynx long; a peculiar 'stripe band' located on dorsal surface has usually its origin in the peristomal groove, after taking an anterior course for a short distance, curves back and runs down posteriorly near right edge and terminates about 1/3 the body length from posterior end; macro nucleus rounded; a
micronucleus; contractile vacuole terminal; free-living or endozoic.
P. nasuta S. (Fig. 315,
gles to
a).

Ovoid; tapering anteriorly; peristome at

to irregular in shape;

right angles or slightly oblique to the edge; trichocysts at right an-

body

surface;

macro nucleus round

about

100/x (80-180/*)

long; sapropelic in brackish water.

body Lynch

HOLOTRICHA

741

(1930) observed this ciliate in salt water cultures in California and

found it to be 70-1 14^ by 31-56/* by 22-37/x. P. minuta Powers (Fig. 315, b). 50-75/x by 36-46/x; in the intestine
of Strongylocentrohis droebachiensis ; the

Bay

of

Fundy

(Powers,

1933).
to Plagiopyla; but with a large embracing the vestibule from right, and a large crescentic motorium at left end of peristome; in the intestine

Genus Lechriopyla Lynch. Similar

internal organella, furcula,

of sea-urchins.

|>i|M?|

Fig. 315. a, Plagiopyla nasuta, X340 (Kahl); b, P. minuta, X400 (Powers); c, Lechriopyla mystax, X340 (Lynch); d, Sonderia pharyngea, X590 (Kirby); e, S. vorax, X310 (Kahl); f, Glathrostoma viminale, X220 (Penard); g, Physalophrya spumosa, X160 (Penard).

L. mystax L. (Fig. 315,

centrotus purpuratus

c).

113-174/x long; in the gut of Stro?igyloto Plagiopyla in general appear-

and

S. franciscanus; California.

Genus Sonderia Kahl. Similar by

2-4/i thick gelatinous

ance; ellipsoid; flattened; peristome small and varied;

body covered

envelope which regulates osmosis, since no

742

PROTOZOOLOGY
Kirby
in the

contractile vacuole occurs (Kahl); with or without a striped band;

trichocysts slanting posteriorly; in salt or brackish water.

(1934) showed that several species of the genus are

common

pools and ditches in salt marshes of California, salinities of which

range 3.5-10 per cent or even up to 15-20 per cent.

S. pharyngea
110/x

Kirby

(Fig. 315, d).

by

48-65/x; gelatinous layer

Ovoid to ellipsoid; flattened; 84about 2/* thick, with bacteria;

about 60 longitudinal ciliary rows, each with 2 borders; peristome about 35/x long, at anterior end, oblique; with closely set cilia from the opposite inner surfaces; cytopharynx conspicuous; spherical macro nucleus anterior, with a micro nucleus; trichocysts (7-9m long) distributed sparsely and unevenly, oblique to body surface; a group of bristle-like cilia at posterior end; often brightly colored because of food material; in salt marsh, California. S. vorax Kahl (Fig. 315, e). Broadly ellipsoid; size variable, 70180/n long; ventral surface flattened; posterior

border of peristomal

cavity extending anteriorly; in salt marsh; California (Kirby, 1934).

Family 7 Clathrostomidae Kahl

Genus Clathrostoma Penard.

Ellipsoid with
;

an oval

pit in anterior

half of the flattened ventral surface, in which occur 3-5 concentric

rows of shorter cilia; cytostome a long slit located at the bottom of this pit; with a basket composed of long fibrils on the outer edge of
the pit in fresh water.
;

Resembles a small Frontonia leucas; macronucleus short sausage-form; 4 micronuclei in a compact group; endoplasm with excretion crystals; 5 preoral ciliary rows; 130-180/x
C. viminale P. (Fig. 315, /).

long; in fresh water.

Family 8 Parameciidae Grobben

Genus Paramecium

Hill

(Paramaecium

tiller).

Cigar- or foot-

shaped; circular or ellipsoid in cross section; with a single macronucleus and 1 to several vesicular or compact micronuclei; peristome

and slightly oblique; in fresh or brackish water. Several Comparative morphology (Wenrich, 1928a; Wichterman, 1953); ciliary arrangement (Lieberman, 1928); pellicular structure (Gelei, 1939); excretory system (Gelei, 1939a); spiral movement (Bullington, 1930); cultivation (Wichterman, 1949). P. caudatum Ehrenberg (Figs. 21, a, b; 43, a-e; 52; 83; 316, a). 180-300ju long; with a compact micronucleus, a massive macronucleus; 2 contractile vacuoles on aboral surface; posterior end bluntly pointed; in fresh water. The most widely distributed species. Cytollong, broad,
species.

HOLOTRICHA

743

ogy and physiology (Miiller, 1932); contractile vacuoles (Dimitrowa, 1928); cytopharynx (Gelei, 1934); calcium and iron (Kruszynski,
1939); nuclear variation (Diller, 1940); re-conjugation (Diller, 1942);

food vacuoles (Bozler, 1924); conjugation (p. 187). P. aurelia E. (Figs. 2, g, h; 57; 89; 100; 101; 102; 316,
long;

6).

120-180/z

two small vesicular micronuclei, a massive macronucleus; two contractile vacuoles on aboral surface; posterior end more rounded
than P. caudatum; amy and hemixis
(p. 190).

in fresh water.
(Diller,

Nutrition (Phelps, 1934); autog-

1936); conjugation and mating types

1 /

Fig. 316. Semi-diagrammatic drawings of nine species of Paramecium showing distinguishing characteristics taken from fresh and stained specimens, X230 (several authors), a, P. caudatum; b, P. aurelia; c, P. multimj,cronucleatum; d, P. bursaria; e, P. putrinum; f, P. calkinsi; g, P. trichium; h, P. polycaryum; i, P. woodruffi.
in oral surface view,

744

PROTOZOOLOGY

316,

P. multimicronucleatum Powers and Mitchell (Figs. 19; 20; 28; 29; c). The largest species, 200-330/x long; three to seven contractile vacuoles; four or more vesicular micronuclei; a single macronucleus;

in fresh water.

Cytology and physiology (Muller, 1932) division and conjugation (Stanghoner, 1932; Koster, 1933); relation to Oikomonas and bacteria in culture (Hardin, 1944).
;

P. bursaria (Ehrenberg) (Figs. 84; 88; 316,

d).

Foot-shaped, some-

what compressed; about 100-1 50^ by 50-60/z; green with zoochlorellae as symbionts; a compact micronucleus; a macronucleus; two contractile vacuoles; in fresh water. Relation between Chlorella and
host
(Parker,

1926;

Pringsheim,

1928);

micronuclear

variation

(Woodruff, 1931); bacteria-free culture (Loefer, 1936); removal of symbionts (Jennings, 1938; Wichterman, 1948); conjugation (p. 189). P. putrinum Claparede and Lacbmann (Fig. 316, e). Similar to P.

and an elongated macronuno zoochlorellae; 80-150m long; in fresh water. P. calkinsi Woodruff (Fig. 316, /). Foot-shaped; posterior end broadly rounded; 100-150/t by 50/x; 2 vesicular micronuclei; 2 conbursaria, but a single contractile vacuole
cleus;
tractile vacuoles; in fresh, brackish

and

salt water.

Ecology, mor-

phology, mating types (Wichterman, 1951).

P. trichium Stokes (Fig. 316, g). Oblong; somewhat compressed; 50-105 (80-90) /i long; a compact micronucleus; two contractile vacuoles deeply situated, each with a convoluted outlet; in fresh
water. Structure and division (Wenrich, 1926); conjugation (p. 190)
(Diller, 1948, 1949).

P. polijcaryum Woodruff and Spencer (Fig. 316, h).

to P. bursaria; 70-1 10/* long; 2 contractile vacuoles;

Form

similar

3-8 vesicular

micronuclei; in fresh water.

P. woodruffi, Wenrich (Fig. 316,
210jtx
i).

Similar to P. polycaryum; 150-

long; 2 contractile vacuoles; 3-4 vesicular micronuclei; brackish

water (Wenrich, 1928). Although Paramecium occurs widely in various freshwater bodies throughout the world and has been studied extensively by numerous investigators by mass or pedigree culture method, there are only a few observations concerning the process of encystment. Blitschli considered that Paramecium was one of the Protozoa in which encystment did not occur. Stages in encystment were however observed in P. bursaria (by Prowazek) and in P. putrinum (by Lindner). In recent years, four observers reported their findings on the encystment of Paramecium. Curtis and Guthrie (1927) give figures in their textbook of zoology, showing the process (in P. caudatuml) (Fig. 317, a-c), while Cleveland (1927) injected Paramecium culture into the rectum

HOLOTRICHA
of frogs

745

and observed that the

ciliate
if

encysted within a thin

P. caudatum
is

mem-

brane. Michelson (1928) found that

kept in Knop-

agar medium, the organism becomes ellipsoidal under certain conditions, later spherical to oval, losing all organellae

except the nuclei,

and develops a thick membrane; the fully formed cyst is elongated and angular, and resembles a sand particle (Fig. 317,/). Michelson considers its resemblance to a sand grain as the chief cause of the cyst having been overlooked by workers. In all these cases, it may however be added that excystment has not been established.

Fig. 317. a-c, encystment in a species of Paramecium (Curtis and Guthrie); d-f, encystment of P. caudatum, X380 (Michelson).

Genus Physalophrya Kahl. Without peristome; but cytostome

cated near the anterior half of body, resembles

lo-

much

that of Para-

mecium; although there is no membrane, a ciliary row occurs in the left dorsal wall of cytopharynx; in fresh water. Taxonomic status is not clear; but because of its general resemblance to Paramecium, the genus with only one species is mentioned here. P. spumosa (Penard) (Fig. 315, g). Oval to cylindrical; highly plastic; cytoplasm reticulated; numerous contractile vacuoles; 150320^ long; in fresh water.

Family 9 Colpodidae Poche

Genus Colpoda

Miiller.

Reniform; compressed; right border semiis

circular; posterior half of the left border often convex; oral funnel in

the middle of flattened ventral side; cytostome

displaced to the

746
right of the

PROTOZOOLOGY
median plane, which leads into peristome cavity and

gives rise dorsally to a diagonal groove; right edge of cytostome bears

a ciliated area, but no protruding

membrane

as in Bryophrya (p.

747); macronucleus spherical or oval, central; a compact micronucleus; a contractile vacuole terminal; in fresh water.

Many

species.

Burt (1940) made a comparative study mentioned here.

C. cucullus

of five species,

which are
with eight

M.

(Fig. 318, a). 40-110/x long; anterior keel

Fig. 318.
e,

a,

Colpoda cucullus;
i,

h, C. inflata; c, C.

maupasi;

d, C.

aspera;

X330 (Burt); f, g, Tillina magna, X100 (Bresslau); h, T. X330 (Turner); Bresslaua vorax, X100 (Kahl); j, Bryophrya bavariensis, X280 (Kahl); k, Woodruffia rostrata, XI 90 (Kahl).
C. steini, all
canalifera,

to 10 indentations; 29-34 ciliary grooves; cilia mostly paired; macro-

nucleus with a stellate endosome; trichocysts rod-form; usually with abundant food vacuoles; in fresh water with decaying plants. C. inflata (Stokes) (Fig. 318, 6). 35-90 M long; anterior keel with 68 indentations;

number

of ciliary grooves (or meridians) 21-24; cilia

mostly
C.

in pairs; in fresh

water among vegetation.

(Fig. 318, c). 35-90/x long;

maupasi Enriques

cytostome about

HOLOTRICHA

747

one-fourth from the anterior end; anterior keel with five indentations; 16-18 meridians; in fresh water.
C. aspera

Kahl

(Fig. 318, d). 12-42/z long;

cytostome about one-

third from the anterior end; 14-16 meridians; anterior keel with five

indentations; in fresh water.

C. steini Maupas (Fig. 318, e). 15-42^; cytostome about two-fifths from the anterior end, and with a bundle of long membranellae; five to six preoral ridges; paired and single cilia; one pair of long caudal cilia; 12 meridians; in fresh water. The organism can live in various organs of the land slug, Agriolimax agrestis (Reynolds, 1936). C. duodenaria Taylor and Furgason. 20-40/x (9-60m) long; 12 longi-

tudinal ciliary rows; 3 postoral rows; 2 long cilia at the posterior

end; long

cilia project out from the cytostome along its posterior margin, forming a "beard"; a contractile vacuole terminal; macronucleus ovoid, with crescentic micro nucleus; division into 2-8 indi-

viduals in division cyst; but no division in trophozoite stage; bacteria-feeder; fresh water.

Encystment (Taylor and Strickland, 1939)

identity (Burt, 1940).

Genus Tillina Gruber. Similar to Colpoda in general appearance and structure; but cytopharynx a long curved, ciliated tube; in fresh
water.
T. magna G. (Fig. 318, /, g). 180-20G> long (Gruber), up to 400 m long (Bresslau) macronucleus oval to rod-shape; micronuclei vesicu;

lar,

highly variable in
in

number

(2-16) (Beers); a contractile vacuole

terminal, with six long collecting canals; division cyst produces four
individuals;

stagnant water and also coprozoic. Morphology

(Gregory, 1909; Beers, 1944, 1945); encystment and excystment

(Beers, 1945, 1946, 1946a).
T. canalifera Turner (Figs. 26; 318, h). 150-200/x by 100-1 50m; resembles magna; but macronucleus ellipsoid, about one-third the

body length; four

to 14 micronuclei, clustered around the macro-

nucleus; a terminal contractile vacuole with seven to nine long

permanent collecting canals; cytoplasm with 3-7/x long refractile rods; in fresh water (Turner, 1937). Cytoplasmic inclusions (Turner,
1940).

Genus Bresslaua Kahl. General body form resembles Colpoda; but cytopharynx large and occupies the entire anterior half. B. vorax K. (Fig. 318, i). 80-250m long; in fresh water. Genus Bryophrya Kahl. Ovoid to ellipsoid; anterior end more or less bent toward left side; cytostome median, about 1/3 from anterior end, its right edge continues in horseshoe form around the posterior end and half of the left edge; anterior portion of left edge of

748

PROTOZOOLOGY

the cytostome with posteriorly directed membrane; macro nucleus oval or spherical; micronuclei; in fresh water.

B. bavariensis K. (Fig. 318,

J*).

50-120ju long.
similar to Chilodonella (p. 731);

Genus Woodruffia Kahl. Form

highly flattened snout bent toward
nal
slit, its left

left; cytostome, a narrow diagoedge with a membranous structure and its right edge with densely standing short cilia; macro nucleus spherical; several (?) micronuclei; contractile vacuole flattened, terminal; in salt water. W. rostrata K. (Fig. 318, k). 120-180ju long; salt water culture with

Oscillatoria.

W.

metabolica Johnson

and Larson

(1938).

Pyriform; 85-400^

long; division cysts 85-155ju in diameter; resting cysts 40-62/i in

diameter; in freshwater ponds. Johnson and Evans (1939, 1940) find two types of protective cysts in this ciliate: "stable" and

"unstable" cysts, formation of both of which depends upon the absence of food. These cysts have three membranes: a thin innermost endocyst, a rigid mesocyst and a gelatinous outer ectocyst.

The protoplasmic mass

vacuoles,

of the stable cyst

is

is

smaller,

and

free

from

and

its

ectocyst

thick,

while that of the unstable

is larger, contains at least one fluid vacuole and its ectocyst very thin. Crowding, feeding on starved Paramecium, increasing the temperature, and increasing the salt concentration of the medium, are said to influence the formation of unstable cysts. The two authors (1941) further reported that when free-swimming individuals were subjected, in the absence of food, to extremes of temperature, high concentrations of hydrogen-ion, and low oxygen tension, unstable cysts were formed; when the oxygen tension decreased, the tendency to encyst increased, even when ample food was present. The unstable cysts are said to remain viable for six months. Excystment is induced by changing the balanced salt solution, by replacing it with distilled water and by lowering temperature from 30 to 20C.

cyst
is

Family 10 Entorhipidiidae Madsen

Genus Entorhipidium Lynch. Triangular in general outline; colorless; large, 155-350/x long; flattened; posterior end drawn out, with
cytostome in depression close to with or without a cross-groove from preoral region; cytopharynx inconspicuous; trichocysts; macronucleus oval to sausage-form; one to several micronuclei; several (exa
bristle; anterior
left;

end bent to

left

anterior border, with long

cilia;

cretory) vacuoles left-ventral; in intestine of the starfish, Strongylocentrotus -pur-pur atus.

Four

species.

HOLOTRICHA

749

E. echini L. (Fig. 319, a). About 253/z by 125m; California. Genus Entodiscus Madsen. Broadly or narrowly lancet-like, without narrowed posterior portion; cytostome small on left narrow side, about 2/5 the body length from anterior end; without trichocysts; macro nucleus central, with a micro nucleus; contractile vacuole subterminal; swimming movement rapid without interruption. Two species. Morphology (Powers, 1933, 1933a). E. indomitus M. (Fig. 319, 6). 80-117/z by 20-23/z; in the intestine
of Strongylocentrotus droebachiensis.

E. borealis (Hentschel) (Fig. 319,

terior end; 105-170/1

c).

Oval; cytostome nearer an-

by

60-115/*; in the gut of Strongylocentrotus

Fig. 319. a, Entorhipidium echini, X270 (Lynch); b, Entodiscus indomitus, X380 (Madsen); c, E. borealis, X380 (Powers); d, Biggaria bermudense, X380 (Powers); e, B. echinometris, X380 (Powers); f, Anophrys elongata, X390 (Powers); g, A. aglycus, X390 (Powers).

750
droebachiensis

PROTOZOOLOGY
and Echinus
in

species in the first-named host

rod which

is

imbedded

Powers (1933) studied this from Maine, and found a supporting the margin along the right wall of the oral
esculentus;
stomatostyle.
thin, posterior

cavity and which he

named

Genus Biggaria Kahl. Scoop-like form; anterior 2/3

tudinal rows; longer
cilia

region thickened, terminating in a rudder-like style; cilia in longi-

on caudal prolongation; cytostome

;

in the

posterior half, opening into a vestibule, into which long cilia project

from the roof aperture to cyto pharynx with 2 membranes contrac;

tile

vacuole subterminal; in the intestine of sea-urchins.

d). 90-185/*

B. bermudense (Biggar) (Fig. 319,

techinus variegatus;

Bermuda

(Biggar),

by 48-82/*; in LyNorth Carolina (Powers).

Powers (1935) found the organism at Tortugas in Lytechinus variegatus,

Centrechinus antillarum, Echinometra lucunter, Tripneustes escu-

lentus

and Astrophyga magnifica.

e).

B. echinometris (B.) (Fig. 319,

Carolina).

80-195/*

by

33-70/*; in Echi-

nometris subangularis (Bermuda) and Lytechinus variegatus (North

Genus Anophrys Cohn. Cigar-shaped;

flexible; longitudinal ciliary

rows; peristome begins near the anterior end, parallel to body axis

and about 1/3 the body length; a row of free cilia on right edge of peristome; cytostome inconspicuous; spherical macro nucleus cenvacuole terminal; in the intestine of sea-urchins. A. elongata Biggar (Fig. 319, /). About 96/t long (Powers); 166m long (Biggar) in the gut of Lytechinus variegatus and Echinometris subangularis; Bermuda (Biggar); Powers (1935) found this species also in the hosts mentioned for Biggaria bermudense.
tral; contractile
;

A. aglycus Powers (Fig. 319, g). 56-120/* by 16-35/*; in the gut of Centrechinus antillarum and Echinometra lucunter; Tortugas (Powers, 1935).

Family

11 Paraisotrichidae

da Cunha
ciliated in

Genus Paraisotricha
less spiral longitudinal

Fiorentini.

Uniformly
cilia at

more or

rows; longer

anterior end; cytostome

near anterior tip; contractile vacuole posterior; in the caecum and

colon of horse.

P. colpoidea F. (Fig. 320,

(Dogiel, 1930).

a).

70-100/*
52-98/*

by

42-60/*. Conjugation

P. beckeri Hsiung (Fig. 320,

b).

by 30-52/* (Hsiung, 1930,

1930a\

HOLOTRICHA
Family 12 Isotrichidae
Blitschli

rai

Genus Isotricha

Stein. Ovoid; flattened; dense longitudinal ciliary

;

rows; cytostome at or near anterior end several contractile vacuoles; reniform macronucleus and a micronucleus connected with, and

suspended by,

fibrils,

karyophore; locomotion with posterior end

directed forward; in the stomach of cattle and sheep.

Fig. 320. a, Paraisotricha colpoidea, X270 (Hsiung); b, P. beckeri, X360 (Hsiung); c, Isotricha prostoma, X500 (Becker and Talbott); d, /. intestinalis, X500 (Becker and Talbott); e, Dasytricha ruminantium, X330 (Becker and Talbott); f, Cyathodinium pirijorme, X1290 (Lucas); g, Blepharocorys uncinata, X540 (Reichenow); h, B. bovis, X850 (Dogiel); i, Charon equi, X570 (Hsiung).

/.

prostoma

S. (Fig. 320, c).

80-195/z by 53-85/x. Cytology

(Camp-

bell, 1929).

I. intestinalis S. (Fig. 320, d). 97-130ju by 68-88/z. Genus Dasytricha Schuberg. Oval, flattened; cilia in longitudinal spiral rows; no karyophore; in the stomach of cattle. D. ruminantium S. (Fig. 320, e). 50-75ju by 30-40^.

752

PROTOZOOLOGY
Family 13 Cyathodiniidae da Cunha

Genus Cyathodinium da Cunha. Conical or pyriform; broad cytostome occupies the entire anterior end and extends posteriorly 1/43/4 the body length; deep with prominent ridges; oral cilia in a single row on left ridge; body cilia comparatively long, confined to anterior half; macro nucleus round or ellipsoid; a micro nucleus; one to several contractile vacuoles; in the caecum and colon of guinea pigs. C. conicum da C. Inverted cone; 50-80ju by 20-30/1 in the caecum of Cavia aperea and C. porcella. C. piriforme da C. (Fig. 320, /). Typical form inverted pyriform; second form conical with tapering anterior end; contractile vacuole posterior; 30-40ju by 20-30ju; in the caecum of Cavia aperea and C. porcella. Occurrence and cytology (Lucas, 1932, 1932a; Nie, 1950).
;

Family 14 Blepharocoridae Hsiung

Genus Blepharocorys Bundle. Oral groove deep, near anterior end; 3 (oral, dorsal and ventral) ciliary zones at anterior end; a caudal ciliary zone; in the caecum and colon of horse or stomach of cattle.

Many

species.

Fig. 321.

The developmental

cycle of Conidiophrys pilisuctor (Chatton

and Lwoff). a, trophont with two tomites; b, freed tomite; c, tomite becoming attached to host's hair; d, lacrymoid trophont; e, spheroid stage;
f,

g,

cucurbitoid stage.

HOLOTRICHA

753

B. uncinata (Fiorentini) (B. equi Schumacher) (Fig. 320, g). With a screw-like anterior process; 55-74/z by 22-30^; in the caecum and colon of horse (Hsiung, 1930a).
B. bovis Dogiel (Fig. 320,
cattle (Dogiel, 1926).
h).

23-37/z

by

10-17//; in the

stomach

of

Genus Charon Jameson. Two caudal

horse or in stomach of ruminants.
C. equi

ciliary zones; in the colon of

Hsiung

(Fig. 320,

i).

30-48m by 10-14ju; in the colon of

horse (Hsiung, 1930, 1930a).

Family 15 Conidophryidae Mohr and LeVeque

(Pilisuctoridae

Chatton and Lwoff)

(Fig. 321).

Genus Conidophrys Chatton and Lwoff

the form attached to host's appendages
pellicle;

Trophont or
with a thick
(b)

(a), cylindrical,

contents divide into two or three (and up to several) smaller

;

bodies which develop into tomites or free-swimming individuals

when

the latter

come

in contact

with the ends of the secretory hairs

Fig. 322. Conidiophrys pilisuctor (Chatton and Lwoff). a, trophonts of ages on an appendage of Corophium acherusicum; b, a stained mature trophont with two formed and one developing tomites, X1330; c, a tomite emerging from trophont, X1330; d, a living tomite, X2230; e, newly attached lacrymoid trophont, X1330.
all

754
of the host,

PROTOZOOLOGY
they become attached through their cytopharynx

(c) and development into the cucurbitoid mature stage (/, g), the organism passes through lacrymoid (d) and spheroid (e) stages; on freshwater amphipods and isopods (Chatton and Lwoff,

lose their cilia; during the

1934, 1936).
L. (Fig. 322). Lacrymoid trophont 12-1 5m by forms 50-60^ long; free-swimming tomites 12 14/i in diameter by 6-7/z high, ciliated and possess a comparatively long cytopharynx; nourishment of trophont through host's hairs; in amphipods and isopods, especially on Corophium acherusicum, France. Mohr and LeVeque (1948) found it on the wood-boring isopods, Limnoria lignorum and Corophium acherusicum in California. C. pilisuctor C.
6-7/*; cucurbitoid

and

References

Beers, C. D.: (1944) The maintenance of vitality the ciliate Tillina magna. Am. Nat., 78:68. (1945) Some factors affecting excystment Tillina magna. Physiol. Zool., 18:80.

in

pure lines of
the
ciliate

in

(1946) History of the nuclei of Tillina magna during division and encystment. J. Morphol., 78:181. (1946a) Tillina magna: etc. Biol. Bull., 91:256. Bozler, E.: (1924) Ueber die Morphologie der Ernahrungsorganelle und die Physiologie der Nahrungsaufnahme bei Paramecium

caudatum. Arch. Protist., 49:163.

Bullington, W. E. (1930) A further study of spiraling in the ciliate Paramecium, etc. J. Exper. Zool., 56:423. Burt, R. L.: (1940) Specific analysis of the genus Colpoda with spe:

the standardization of experimental material. Micr. Soc, 59:414. Kidder, G. W. and Claff, C. L.: (1941) Nuclear reorganization in the family Colpodidae. J. Morphol., 69:537. Campbell, A. S.: (1929) The structure of Isotricha prostoma. Arch. Protist., 66:331. Chatton, E. and Lwoff, A.: (1934) Sur un infusoire parasite des poils secreteurs des crustaces Edriophtalmes et la famille nouvelle des Pilisuctoridae. C. R. Acad. Sc, 199:696. (1936) Les Pilisuctoridae. Bull. biol. France et Belg., 70:86. Claff, C. L., Dewey, Virginia C. and Kidder, G. W.: (1941) Feeding mechanisms and nutrition in three species of Bresslaua. Biol. Bull., 81:221. Cleveland, L. R. (1927) The encystment of Paramecium in the recta of frogs. Science, 66:221. Curtis, W. C. and Guthrie, Mary J.: (1927) Textbook of general zoology. New York. Diller, W. F.: (1936) Nuclear reorganization processes in Paramecium aurelia, etc. J. Morphol., 59: 11.
cial reference to

Tr.
,

Am.

HOLOTRICHA

755

(1940) Nuclear variation in Paramecium caudatum. Ibid., 66:605. (1942) Re-conjugation in Paramecium caudatum. Ibid., 70:

229. (1948) Nuclear behavior of Paramecium trichium during conjugation. Ibid., 82:1. (1949) An abbreviated conjugation process in Paramecium trichium. Biol. Bull., 97:331. Dimitrowa, A.: (1928) Untersuchungen liber die iiberzahligen pulsierenden Vakuolen bei Paramecium caudatum. Arch. Protist.,

64:462.

Dogiel, V.: (1926) Une nouvelle espece du genre Blepharocorys, B. bovis, etc. Ann. Parasitol., 4:61. (1930) Die prospektive Potenz der Syncaryonderivate an der Conjugation von Paraisotricha erlautert. Arch. Protist., 70:
497.

Gelei,

J. v.: (1934) Der feinere Bau des Cytopharynx von Paramecium und seine systematische Bedeutung. Ibid., 82:331. (1939) Das aussere Stiitzgerustsystem des Paramecium-

zum Bau und zu der Funktion des Exkretionssystems von Paramecium. Ibid., 92:385. Gregory, Louise H.: (1909) Observations on the life history of Tillina magna. J. Exper. Zool., 6:383. Hardin, G.: (1944) Symbiosis of Paramecium and Oikomonas. Ecology, 25:304.
S.: (1930) Some new ciliates from the large intestine of the horse. Tr. Am. Micr. Soc, 49:34. (1930a) A monograph on the Protozoa of the large intestine of the horse. Iowa State College J. Sc, 4:356. Jennings, H. S.: (1938) Sex reaction types and their interrelations Proc. Nat. Acad. Sc, 24:112. in Paramecium bursaria. I. Johnson, W. H. and Evans, F. R. (1939) A study of encystment in the ciliate, Woodruffia metabolica. Arch. Protist., 92:91. (1940) Environmental factors affecting cystment in Woodruffia metabolica. Physiol. Zool., 13:102. (1941) A further study of environmental factors affecting cystment in Woodruffia metabolica. Ibid., 14:227. and Larson, Enid: (1938) Studies on the morphology and life history of Woodruffia metabolica, n. sp. Arch. Protist., 90:

korpers. Ibid., 92:245. (1939a) Neue Beitrage

Hsiung, T.

383.

Kidder, G. W. and Claff, C.

of

L.: (1938) Cytological investigations

in California.

Colpoda cucullus. Biol. Bull., 74:178. Kirby, H. Jr.: (1934) Some ciliates from salt marshes
:

Arch. Protist., 82:114. Koster, W. (1933) Untersuchungen iiber Teilung und Conjugation bei Paramecium multimicronucleatum. Ibid., 80:410. Kruszynski, J.: (1939) Mikrochemische Untersuchungen des veraschten Paramecium caudatum. Ibid., 92:1. Lackey, J. B.: (1925) The fauna of Imhoff tanks. Bull. N. J. Agr. Exper. St., No. 417.

756
:

PROTOZOOLOGY

Lieberman, P. R. (1929) Ciliary arrangement in different species of Paramecium. Tr. Am. Micr. Soc, 48:1. Loefer, J. B. (1936) Bacteria-free culture of Paramecium bursaria and concentration of the medium as a factor in growth. J. Exper.
:

Zool., 72:387.
S.: (1932) A study of Cyathodinium piriforme. Arch. Protist., 77:64. (1932a) The cytoplasmic phases of rejuvenescence and fisIbid., 77:406. sion in Cyathodinium piriforme. II. Lynch, J.: (1929) Studies on the ciliates from the intestine of Univ. California Publ. Zool., 33:27. Strongylocentrotus. I. (1930) II. Ibid., 33:307. Michelson, E.: (1928) Existenzbedingungen und Cystenbildung bei Paramecium caudatum. Arch. Protist., 61:167. Mohr, J. L. and LeVeque, J. A. (1948) Occurrence of Conidophrys, etc. J. Parasitol., 34:253. MiiLLER, W.: (1932) Cytologische und vergleichend-physiologische Untersuchunger liber Paramecium multimicronucleatum und P. caudatum, etc. Arch. Protist., 78:361. Nie, D.: (1950) Morphology and taxonomy of the intestinal Protozoa of the guinea-pigs, Cavia porcella. J. Morphol., 86:381. Parker, R. C: (1926) Symbiosis in Paramecium bursaria. J. Exper. Zool, 46:1. Powers, P. B. A. (1933) Studies on the ciliates from sea urchins. I. Biol. Bull., 65:106. Ibid., 65:122. (1933a) II. (1935) Studies on the ciliates of sea urchins. Papers Tortugas Lab., 29:293. Pringsheim, E. G.: (1928) Physiologische Untersuchungen an Paramecium bursaria. Arch. Protist., 64:289. Reynolds, B. D.: (1936) Colpoda steini, a facultative parasite of the land slug, Agriolimax agrestis. J. Parasitol., 22:48. Stranghoner, E.: (1932) Teilungsrate und Kernreorganisationsprozess bei Paramecium multimicronucleatum. Arch. Protist., 78 302 Stuart, C. A., Kidder, G. W. and Griffin, A. M.: (1939) Growth Physiol. Zool., 12:348. studies on ciliates. III. Taylor, C. V. and Furgason, W. H.: (1938) Structural analysis of Colpoda duodenaria sp. nov. Arch. Protist., 90:320. and Strickland, A. G.: (1939) Reactions of Colpoda duoPhysiol. Zool., 12:219. denaria to environmental factors. II. Turner, J. P.: (1937) Studies on the ciliate Tillina canalijera n. sp. Tr. Am. Micr. Soc, 56:447. (1940) Cytoplasmic inclusions in the ciliate Tillina canalijera. Arch. Protist. 93 255. Wenrich, D. H.: (1926) The structure and division of Paramecium trichium. J. Morphol. Physiol., 43:81. (1928) Paramecium woodruffi n. sp. Tr. Am. Micr. Soc, 47:

Lucas, Miriam

256. (1928a) Eight well-defined species of 275.

Paramecium.

Ibid., 47:

HOLOTRICHA
Wichterman, R.
113.
:

757

(1948) The biological effects of x-rays on mating types and conjugation of Paramecium bursaria. Biol. Bull., 94:
sterilization of

(1949) The collection, cultivation, and mecium. Proc. Penn. Acad. Sc, 23:151. (1951)

Para-

ecology, cultivation, structural characteristics of Paramecium calkinsi. Ibid., 25:51. (1953) The biology of Paramecium. New York. Woodruff, L. L.: (1921) The structure, life history and intrageneric relationships of Paramecium calkinsi, sp. nov. Biol. Bull, 41:

The

and mating types

171.

(1931)

Micronuclear variation in Paramecium bursaria.

Quart.

J.

Micr.Sc, 74:537.

Chapter 35

Order

Holotricha Stein (continued)

Suborder 4 Hymenostomata Delage and Herouard

Family 1 Frontoniidae Cytostome not connected with peristome Oytostome at end or bottom of peristome Peristome sickle-form, ciliated slit; sunk at right angles to body surface Family 2 Ophryoglenidae (p. 767) Peristome long, begins at anterior end of body Peristome with a one-layered membrane which forms a pocket surrounding cytostome on right edge and a row of cilia or memFamily 3 Pleuronematidae (p. 769) brane on left
Peristome otherwise Peristome with 2 one-layered membranes; no distinct ectoplasmic pocket around cytostome. .Family 4 Cohnilembidae (p. 771) Peristome furrow either covered densely with cilia, besides an undulating membrane on right edge, or with only a thick undulating membrane on the right edge

Family 5 Philasteridae

(p.

771)

Family

Frontoniidae Kahl

Genus Frontonia Ehrenberg. Ovoid to ellipsoid; anterior end more broadly rounded than posterior end; flattened; oral groove lies in anterior third or more or less flattened ventral surface, to right of
median
rior

with pointed anterior and truncate posteedge is more curved than right edge, and posteriorly becomes a prominent ectoplasmic lip; cytostome with a complex organization (on left edge a large undulating membrane composed of 3 layers, each being made up of 4 rows of cilia; on right, semimembranous groups of cilia; 3 outer rows of cilia from the postoral suture; along this suture ectoplasm is discontinuous so that large food matter is taken in; with a small triangular ciliated field posterior to cytostome and left of suture) a long narrow postoral groove which is ordinarily nearly closed cytopharynx w ith numerous strong fibrils; ciliary rows close and uniform; ectoplasm with numerous fusiform trichocysts; macro nucleus oval; one to several micro nuclei; 1-2 contractile vacuoles, with collecting canals and an external pore;
line; lancet-like
left

end;

in fresh or salt water. Species identification

and movement (Bullingfila-

ton, 1939); trichocysts (Kriiger, 1931).

F. leucas E. (Figs. 2,

i,

j; 323, a-c).

150-600^ long; feeds on

mentous

algae,

but

may

take in Arcella and even large amoebae

(Fig. 323, d). 75-100jn

(Beers, 1933);

among

algae in fresh water.

F. branchiostomae

Codreanu

by

55-95/x;

commensal

in the branchial cavity of

Amphioxus.

758

HOLOTRICHA
Genus Disematostoma Lauterborn. Somewhat
tonia; pyriform;

759

similar to Fronwith broadly rounded, truncate or concave anterior end and bluntly pointed narrow posterior end; preoral canal wide; a dorsal ridge in posterior region of body; macro nucleus sausageform; a micro nucleus; contractile vacuole in middle of body, with

long collecting canals; in fresh water.

Fig. 323. a-c, Frontonia leucas (Bullington)

(a,

aboral view showing a

contractile vacuole, collecting canals, macronucleus, four micronuclei and trichocysts, X220; b, oral view, showing the cytostome with undulating

membrane and

groove, X165;

c,

portion of pellicle with wart-like projec-

tions over trichocysts); d, F. branchiostomae,

atostoma butschlii,

(Kahl); f, Lembadion bullinum, Tetrahymena pyriformis, X950 (Furgason).

X340

X490 (Codreanu); e, DisemX170 (Kahl); g,

760

PROTOZOOLOGY
biitschlii L. (Fig.

D.

323,

e).

135-155^ long; with or without zooside convex, ventral side

its left

chlorellae; in fresh water.

Genus Lembadion Perty. Oval; dorsal

concave; cytostome 3/4-4/5 the body length; on

with a large

membrane composed of many ciliary rows and on its right, numerous narrow rows of short free cilia; an undulating membrane and ciliary
rows near posterior end; contractile vacuole in mid-dorsal region with a long tubule opening at posterior-right side; close ciliation uniform; macronucleus ellipsoid, subterminal; a micro nucleus; long
caudal
long.
cilia; in fresh

water.

L. bullinum P. (Fig. 323, /). 120-200^ long; posterior cilia 40-50/x

(1941). Pyriform; small forms; unirows or meridians 17-42; 2 postoral meridians; preoral suture straight; cytostome small, close to anterior end, pyriform; its axis parallel to body axis; inconspicuous ectoplasmic ridge or flange on the left margin of mouth; an undulating membrane on right side and 3 membranellae on left of the cytostome; a single contractile vacuole; macronucleus ovoid; micronucleus absent in some species; in fresh water or parasitic. Corliss (1952, 1952a) made a comparative study of different strains and allied forms. T. pyriformis (Ehrenberg) (T. geleii Furgason) (Figs. 323, g; 324, a-c). 59 strains (Corliss, 1952a) 40-60/x long; 17-23 ciliary meridians; pyriform cytostome about 1/10 the body length; with or without micronucleus; bacteria-feeder; in fresh water (Corless, 1952, 1952a). Bacteria-free or pure culture (Kidder, 1941) (p. 884). T. vorax (Kidder, Lilly and Claff) (Glaucoma vorax K. L. and C.)

Genus Tetrahymena Furgason

ciliation; ciliary

form

(Fig. 39).

Form and

size

vary; bacteria-feeders elongate pyriform,

sterile particle-feeders, 60-80/z long;

50-75ju long; saprozoic forms fusiform, 30-70/z long, decreasing in

size

with the age of culture;

carnivores and cannibals broadly pyriform, 100-250^ long; 19-21

ciliary meridians;
line irregular;

macronucleus ovoid, central; in carnivores, out-

apparently without micronucleus; pond water. T. limacis (Warren). In the liver and other visceral organs of the gray garden slug, Deroceras agreste; 33-68 (55) n by 18-35(27)//;
those from cultures measure 28-68(44) n

by 1 7-42(27) /x; the

;

parasitic

phase is cucumber-shaped with apiculate anterior end the free-living organisms are pyriform, somewhat pointed anteriorly; cytostome at about 1/4 from the anterior end, with an undulating membrane and three membranelles; 33-37 ciliary rows (Kozloff, 1946). Genus Leucophrys Ehrenberg. Broadly pyriform; cytostome large, pyriform, with its axis parallel to body axis; ectoplasmic flange along

HOLOTRICHA
left
left

761

margin; undulating membrane on right and 3 membranellae on of mouth; 5 postoral ciliary meridians; macronucleus ovoid; a micronucleus; fresh water.
L. patula E. (Fig. 324, d-f). Broadly pyriform; 80-160/x long;

1/3 the body length; 40-45 ciliary meridians; macronucleus irregularly

ovoid; a micronucleus attached to macronucleus; carnivorous, but

occasionally small forms occur; cytostome pyriform, about

may
sis

be cultured in

sterile

media (Kidder) fresh water. Morphogene;

(Faur6-Fremiet, 1948).

Genus Glaucoma Ehrenberg (Dallasia Stokes). Ovoid or ellipsoid; cytostome about one-fourth the body length, near anterior end, ellipsoid; cytostome with an inconspicuous undulating membrane

Fig. 324. a-c, Tetrahymena pyriformis (a, X535 (Kidder); b, c, cytostomal structure (Furgason)); d-f, Leucophrys patula (d, a well-fed animal, X280 (Maupas); e, a diagram, X535 (Kidder); f, cytostome (Furgason)); g, h, Glaucoma scintillans (g, a diagram, X535 (Kidder); h, cytostome (Furgason)); i, j, Colpidium colpoda (i, X180 (Kahl); j, cytostome (Furgason)) k, C. campylum, X535 (Kidder) 1, C. echini, X385 (Powers) m, Paraglaucoma rostrata, X400 (Kahl); n, Malacophrys rotans, X500
;

(Kahl).

762

PROTOZOOLOGY
left;

on right and 3 membranellae on

ectoplasmic ridge on right bor-

der of mouth; ciliation uniform; 30-40 ciliary meridians; 7 postoral meridians; macro nucleus rounded; a micro nucleus; a contractile
vacuole; with or without
long;
1

or more caudal bristles; fresh water.

g, h). Ovate with rounded ends; 45-75 ix U-shaped cytostome, about one-fourth the body length, oblique; ectoplasmic flange and 3 membranellae conspicuous; a contractile vacuole in posterior one-third; macronucleus oval, central;

G. scintillans E. (Fig. 324,

a micronucleus bacteria-feeder; in fresh water. Bacteria-free culture

;

(Kidder, 1941); division (Kidder and Diller, 1934)

Genus Colpidium

Stein.

Elongate reniform;

ciliary

meridians
tri-

variable in number, but typically one postoral meridian; small

angular cytostome one-fourth from anterior end toward right side; a small ectoplasmic flange along right border of cytostome which

shows an undulating membrane on right and 3 membranellae on left; rounded macronucleus; a micronucleus; a contractile vacuole; fresh or salt water or parasitic.
C. colpoda (Ehrenberg) (Tillina helia Stokes) (Figs. 10, c; 324,
j). Elongate reniform; 90-1 50m long; cytostome about onetenth the body length 55-60 ciliary meridians; preoral suture curved to left; macronucleus oval, central; a micronucleus; fresh water.
i,
;

Bacteria-free culture (Kidder, 1941); division (Kidder and Diller,

1934); effect of food bacteria on division (Burbank, 1942).

C.

campylum

(Stokes) (Fig. 324, k). Elongate reniform; 27-30

ciliary meridians; preoral suture

curved to right; 50-70 m long; in

Diller, 1934).

fresh

and brackish water. Division (Kidder and

C. striatum S.

Similar to the last species; contractile vacuole

further posterior; 50^ long; in standing water.

centrotus lividus; 37-64(55)/*

In the intestinal caeca of Strongylo21-28(25)/*; 24 longitudinal ciliary rows; cytostome at anterior third (Powers, 1933). Genus Paraglaucoma Kahl. Somewhat similar to Glaucoma; but
C. echini (Russo) (Fig. 324,
I)
.

by

without perioral ectoplasmic ridge; a membrane on right ridge of the cytostome; anterior end drawn out to a point in profile, posterior end rounded; a stiff posterior bristle; a contractile vacuole; rapid
zig-zag

movement. One

species.

P. rostrata K. (Fig. 324, m). 60-80ix long; in fresh water (often in

dead rotiferan body); California, Wisconsin (Kahl). Genus Malacophrys Kahl. Ellipsoid or cylindrical; plastic; cilia uniformly close-set in longitudinal rows; slit-like cytostome at anterior extremity in fresh water.
;

M.

rotans K. (Fig. 324, n). Oval; close

and dense

ciliation; spheri-

HOLOTRICHA
cal
ole;

763

macro nucleus

central; a micro-nucleus; a single contractile vacu-

body 40-50/x long; fresh water. Genus Espejoia Burger (Balantiophorus Penard).
;

Ellipsoid; an-

end obliquely truncate; large cytostome at anterior end; postoral groove on ventral side, 1/4-1/3 the body length a conspicuous membrane on the left edge of groove; in gelatinous envelope of eggs of insects and molluscs.
terior

E. musicola (P.) (Fig. 325, a). Elongate; right side flat, left side convex; 80-100^ long (Penard); 70-80m long and dimorphic (FaureFremiet and Mugard, 1949).

Genus Cryptochilidium Schouteden (Cryptochilum Maupas). Ellipsoid;

with rounded anterior end, posterior end pointed in

cilia

profile;

highly compressed; uniform and close ciliation; cytostome near middle;

one or more longer

at posterior end; contractile vacuole

posterior; macronucleus round; a micronucleus;

commensal. Several

species (Powers, 1933, 1935).

C. echini

(Maupas)

(Fig. 325, b).

70-140m long; in the gut of Echi-

nus

lividus.

Genus Eurychilum Andre. Elongate ellipsoid; anterior end somewhat narrowed; cilia short; dense ciliation not in rows; contractile
vacuole terminal; macronucleus band-form; cytostome about 2/5 from anterior end and toward right, with a strong undulating membrane on left; no cyto pharynx; actively swimming. One species.
E. actiniae A. (Fig. 325,
cavity of Sagartia parasitica.
c).

About

155/x long; in gastrovascular

Genus Monochilum Schewiakoff. Ovoid to ellipsoid; medium uniform and dense ciliation in rows; oblong cytostome left of median line, in about 1/4 the body length from anterior end; short cyto pharynx conical, with an undulating membrane; contractile
large;

vacuole near middle; in fresh water.

M. frontatum
flattened,

S.

(Fig. 325, d). Anterior

end broader; ventrally

ellipsoid;

dorsally

micronucleus; feeds

somewhat convex; macronucleus on algae; 80/* by 30/u.

Genus Dichilum Schewiakoff. Similar to Monochilum; but membrane on both edges of the cytostome; in fresh or salt water. D. cuneiforme S. (Fig. 325, e). Ellipsoid; cytostome about 1/5 the body length from anterior end; right membrane larger than left; small cytopharynx; macronucleus ellipsoid; about 40/x by 24ju; in
fresh water.

Genus Loxocephalus Eberhard. Ovoid to cylindrical; sometimes compressed; crescentic cytostome on slightly flattened area near anterior end, with 2 membranes; often a zone of cilia around body;

764

PROTOZOOLOGY
1 (or

usually

more) long caudal cilium; endoplasm granulated, yel-

lowish to dark brown; macronucleus ovoid; a single contractile

vacuole; in fresh or brackish water.

Many species.

L. plagius (Stokes) (Fig. 325,/). 50-65/* long; nearly cylindrical;

15-16 ciliary rows; endoplasm usually darkly colored; in fresh water

among decaying
like ends;

vegetation.
to Loxocephalus;

Genus Balanonema Kahl. Similar

cytostome

but with plug-

difficult to see;

a caudal cilium; macronucleus

echini,

a, Espejoia musicola, X300 (Penard); b, Cryptochilidium X380 (Powers); c, Eurychilum actiniae, X360 (Andre); d, Monochilum frontatum, X440 (Schewiakofif) e, Dichilum cuneiforme, X700 (Schewiakoff); f, Loxocephalus plagius, X380 (Stokes); g, Balanonema biceps, X600 (Penard); h, Platynematum sociale, X500 (Kahl); i, Saprophilus agitatus, X450 (Stokes); j, S. muscorum, X440 (Kahl); k, Cinetochilum margaritaceum, X440 (Kahl).

Fig. 325.

oval; contractile-vacuole; ciliation uniform or broken in the middle

zone fresh water. B. biceps (Penard) (Fig. 325, g). Ellipsoid; no cilia in the middle region; contractile vacuole central; macronucleus posterior to it;
;

42-50ju long.

Genus Platynematum Kahl. Ovoid or ellipsoid; highly flattened; with a long caudal cilium; contractile vacuole posterior-right; small

HOLOTRICHA
cytostome more or
ciliary

765

less toward right side, with 2 outer membranes; furrows horseshoe-shaped; in fresh or salt water.
h).

P. sociale (Penard) (Fig. 325,

Anterior hall more flattened;

ventral side concave; cytostome in the anterior third; yellowish and

granulated; 30-50/x long; sapropelic in fresh and brackish water.

Genus Saprophilus Stokes. Ovoid or pyriform; compressed, cytostome in anterior 1/4-1/3 near right edge, with two membranes; macro nucleus spherical; contractile vacuole posterior; in fresh water. S. agitatus S. (Fig. 325, i). Ellipsoid; ends bluntly pointed; compressed; plastic; close striation; about 4G> long; in fresh water in decomposing animal matter such as Gammarus. S. muscorum Kahl (Fig. 325, j). Cytostome large, with a large membrane; trichocysts; contractile vacuole with a distinct canal; body about 35ju long; in fresh water. Genus Cinetochilum Perty. Oval to ellipsoid; highly flattened; cilia on flat ventral surface only; cytostome right of median line in posterior half, with a membrane on both edges which form a pocket; oblique non-ciliated postoral field leads to left posterior end; with 3^1 caudal cilia; macro nucleus spherical, central; contractile
vacuole terminal; in fresh or salt water. Neuroneme system (Gelei,
1940).
C. margaritaceum P.
(Fig.

325, k).

15-45/x long; in fresh

and

brackish water.

Genus Dexiotrichides Kahl (Dexiotricha Stokes). Reniform; commembranes; long cilia sparse; a special oblique row of cilia; a single caudal cilium; contractile vacuole terminal; spheroidal macro nucleus anterior; a micronucleus in fresh water. One species. D. centralis (Stokes) (Fig. 326, a). About 30-45/i long; in decaying
pressed; cytostome near middle, with two
;

vegetable matter.

Genus Cyrtolophosis Stokes. Ovoid or ellipsoid; with a mucilaginous envelope in which it lives, but from which it emerges freely; cytostome near anterior end with a pocket-forming membrane; on right side a short row of special stiff cilia, bent ventrally; sparse
ciliation spiral to posterior-left; spherical

macro nucleus

central; a

contractile vacuole; in fresh water.

C. mucicola S. (Fig. 326,
b).

25-28m long; in infusion of leaves.

broad girdles of
cilia;

Genus Urocentrum Nitzsch. Short cocoon-shaped, constricted

in the middle; ventral surface flat; 2
cilia at

fused

posterior end; with a zone of short cilia in the constricted

area; cytopharynx with a

rates

stiff ectoplasmic membrane which sepatwo undulating membranes; macronucleus horseshoe-shaped,

766

PROTOZOOLOGY

posterior; a micronucleus; contractile vacuole terminal, with eight

long collecting canals which reach the middle of body; in fresh water.
c). 50-80/z long; unique movement. and Diller, 1934). Genus Urozona Schewiakoff. Ovoid, both ends broadly rounded; a distinct constriction in the ciliated middle region; ciliary band composed of 5-6 rows of cilia, directed anteriorly and arranged longitudinally; cytostome with a membrane; rounded macro nucleus and a

U. turbo (Miiller) (Fig. 326,

Fission (Kidder

micronucleus posterior contractie vacuole subterminal ;in freshwater.

;

Fig. 326. a, Dexiotrichides centralis, X500 (Kahl); b, Cyrtolophosis mucicola, X670 (Kahl); c, Urocentrum turbo, X200 (Biitschli); d, Urozona butschlii, X440 (Kahl); e, Uronema marinum, X490 (Kahl); f, g, U. pluri-

caudatum,
stein);
1,

Stokesia vernalis,

X940 (Noland); h, Homalogastra setosa, X450 (Kahl); i, j, X340 (Wenrich); k, Ophryoglena collini, X150 (Liechten0. pyriformis, X180 (Rossolimo); m, 0. intestinalis, X55

(Rossolimo).

HOLOTRICHA
U.
biitschlii S. (Fig.
;

767

326, d). 20-25^ long (Kahl); 30-40/i (Schewito elongate ovoid; slightly flat-

akoff ) in stagnant water.

Genus Uronema Dujardin. Oval

tened; anterior region not ciliated; inconspicuous peristome with ciliated right edge; cytostome on the ventral side close to left border
in the anterior half,

indistinct;

minal; in
1940).

with a small tongue-like membrane; cytopharynx macronucleus spherical, central; contractile vacuole tersalt or fresh water. Comparison with Cyclidium (Parducz,
(Fig. 326, e). 30-50/x long; in salt

U.

marinum D.

water among

algae. Structure (Parducz, 1939).

U. pluricaudatum No land (Fig. 326, /, g). Body appears to be twisted in dorsal view, due to a spiral depression that runs obliquely

down toward cytostome; with about

Florida (Noland, 1937).

8 caudal

cilia; in salt

water;

a long caudal cilium; a group of

fresh water.

Genus Homalogastra Kahl. Broad fusiform; furrows spiral to left; cilia on right and left side of it;

macronucleus spherical, anterior; contractile vacuole posterior; in

H. setosa K. (Fig. 326, h). About 3(V long; fresh water. Genus Stokesia Wenrich. Oblique cone with rounded
longer
cilia,

angles; flat

anterior surface uniformly ciliated; with peristome bearing zones of

at the
girdle of longer cilia

diameter; pellicle

bottom of which is located the cytostome; a around the organism in the region of its greatest finely striated; with zoochlorellae; trichocysts;

free-swimming; in freshwater pond. One species (Wenrich, 1929). S. vemalis W. (Fig. 326, i,j). 100-16G> in diameter; macronucleus; 2-4 micronuclei; fresh water.

Family 2 Ophryoglenidae Kent

Ellipsoidal to cylindrical; ends rounded or attenuated; preoral depression in form of '6' due to an ectoplasmic membrane extending from the left edge, cilia on the right edge; cytostome deep-seated; 1 (or 2) contractile vacuole with long radiating canals, opens through pores on right ventral side; macronucleus of various forms with several endosomes; a micronucleus; fresh or salt water or parasitic. Many species. 0. collini Lichtenstein (Fig. 326, k). Pyriform; macronucleus horseshoe-shape; 200-300^ by 120-230/z; in the caecum of Baetis
larvae.

Genus Ophryoglena Ehrenberg.

O. parasitica Andre. Ovoid; dark; micronucleus (?); 170-350/x

by

180-200/z; in the gastro vascular cavity of Dendrocoelum lacteum.

768

PROTOZOOLOGY
l).

0. pyriformis Rosso limo (Fig. 326,

Flask-shape; 240-300^ long;

in the gastro vascular cavity of various Turbellaria.

0. intestinalis R. (Fig. 326, ra).

est

Up

to 1.5

mm. by 450-500/*;

small-

60m long; in the gastro vascular cavity of Dicotylus sp. 0. atra Lieberkuhn. Oval, posterior end broadly rounded; 300500/x long; grayish; filled with globules; cytostome near anterior end; macro nucleus elongated; a contractile vacuole; trichocysts; stagnant
fresh water.

Genus Deltopylum Faure-Fremiet and Mugard.

form
ciliation

Cylindrical; uni-

on about 70

ciliary rows; a triangular

cytostome in the

anterior fourth, with a paroral undulating

membrane on

three adoral

membranes; a

contractile vacuole

pore being located in a depression of pellicle

right and on mid-right side, a above it; macronucleus

Fig. 327.
b,

a, Deltopylum rhabdoides, X665 (Faur6-Frenriet and Mugard); Pleuronema crassum, X240 (Kahl); c, P. anodontae, X290 (Kahl); d, e,

P. setigerum,

marinum, X400 (Noland);

f, P. coronatum, X540 (Noland); g, P. Cyclidium litomesum, X300 (Stokes); i. Cristigera phoenix, X500 (Penard); j, C. media, X400 (Ka,hl),

X540 (Noland);
h,

HOLOTRICHA
Fremiet and Mugard, 1946).

769

irregularly ribbon-like; five or six micronuclei; in fresh water (Faure"-

by and curved, posterior end rounded; the organism grows well on the gut of Chironomus larvae
D. rhabdoides F. and
(Fig. 327, a). Cylindrical; 150-180/z

M.

40-45/z; anterior end slightly attenuated

in laboratory.

Family 3 Pleuronematidae Kent

Genus Pleuronema Dujardin. Ovoid to ellipsoid; peristome begins at anterior end and extends for 2/3 the body length; a conspicuous

membrane

at both edges; semicircular swelling to left near oral area; no cyto pharynx; close striation longitudinal; one to many posterior sensory stiff cilia; macro nucleus round or oval; a micro nucleus; a

contractile vacuole; trichocysts in

also

some species; fresh or salt water, commensal in freshwater mussels. P. crassum D. (Fig. 327, b). 70-120/x long; somewhat compressed; Woods Hole (Calkins). P. anodontae Kahl (Fig. 327, c). About 55m long; posterior cilium about 1/2 the body length in Sphaerium, Anodonta.
;

P. setigerum Calkins (Fig. 327,

land)

d, e).

Ellipsoid; flattened; ventral

surface slightly concave; about 25 ciliary rows; 38-50/z long (No;

in salt water; Massachusetts, Florida.

. ;

P. coronatum Kent (Fig. 327, /) Elongate ovoid both ends equally rounded; caudal cilia long; about 40 ciliary rows; 47-75/x long

(Noland, 1937) in fresh and salt water; Florida.

;

marinum D. (Fig. 327, g). Elongate ovoid; trichocysts distinct; caudal cilia medium long; about 50 ciliary rows; 51-126ju long
P.

(Noland) in
;

salt

water; Florida.
Mtiller.

Genus Cyclidium
with refractile

Small,

15-60ju long; ovoid; usually

with a caudal cilium; peristome near right side; on its right edge occurs a membrane which forms a pocket around cytostomal groove and on its left edge either free cilia or a membrane which unites with that on right; no semicircular swelling on left of oral region; round macronucleus with a micro nucleus; conpellicle;

tractile

vacuole posterior; fresh or

salt water.

Numerous

species. 3

species in sea urchin (Powers,

1935); comparison with

Uronema

(Parducz, 1940).
C. litomesum Stokes (Fig. 327, h).
slightly
less

About 40m long; dorsal surface convex with a depression in middle; ventral surface more or
cilia

concave;

long; in fresh water.

Genus

Cristigera Roux. Similar to Cyclidium;

much compressed

70

PROTOZOOLOGY
line;

with a postoral depression; peristome closer to mid-ventral

fresh or salt water. Several species.
C. phoenix
C.

Penard (Fig. 327, i). 35-50^ long; fresh water. media Kahl (Fig. 327, j). 45-50m long; in salt water. Genus Ctedoctema Stokes. Similar to Cyclidium in body form; peristome nearer median line, diagonally right to left; right peri-

Wto>

Fig. 328. a, Ctedoctema acanthocrypta, X840 (Kahl); b, Calyptotricha pleuronemoides, X180 (Kahl); c, Histiobalantium natans, X420 (Kahl); d, H. semisetatum, X270 (Noland); e, Pleurocoptes hydr actiniae, X470 (Wallengren); f, Cohnilembus fusifor?nis, X560 (Kahl); g, C. caeci, X390 (Powers); h, Philaster digitifomris, X220 (Kahl); i, P. armata, X240 (Kahl); j, Helicostoma buddenbrocki, X190 (Kahl).

stomal ridge with a

sail-like

membrane which surrounds the

cyto-

stome at

its

posterior end; trichocysts throughout; fresh water.

35ju long; in fresh

C. acanthocrypta S. (Fig. 328, a). Ovoid; anterior end truncate;

macro nucleus round, anterior; about

vegetation.

water among

Genus Calyptotricha

Phillips.

Somewhat resembles Pleuronema or

is

Cyclidium; but dwelling in a lorica which

opened at both ends;

with zoochlorellae; fresh water. C. pleuronemoides P. (Fig. 328,

b).

Lorica about 85/* high; body

HOLOTRICHA
about
water.
50ju long; Kellicott's (1885)

771

form

is

more elongated;

in fresh

Genus Histiobalantium Stokes. Ovoid; ventral

ciliation

side flattened;

uniform; long

stiff cilia

distributed over the

body

surface;

peristome deep; both anterior and posterior regions with a welldeveloped membrane, connected with the undulating membrane; macro nucleus in 2 parts; 1-2 micro nuclei; several contractile vacuoles distributed
;

fresh water.

H. natans (Claparede and Lachmann) (Fig. 328, c). 70-1 10/x long. H. semisetatum Noland (Fig. 328, d). Elongate ellipsoid; posterior end bluntly rounded; macro nucleus spherical; longer cilia on posterior half only; contractile vacuoles
salt

on dorsal

side; 126-205/x long;

water; Florida (Noland, 1937).

side hemispher-

Genus Pleurocoptes Wallengren. Ovoid, dorsal

ical,

ventral side flattened; peristome large, reaching the posterior

1/3; cyto pharynx indistinct; longer cilia along peristome; macro-

nucleus spherical; several micronuclei; contractile vacuole terminal;

ectocommensal.
P. hydractiniae
echinata.

W.

(Fig. 328, e). 60-70/x long;

on Hydractinia

Family 4 Cohnilembidae Kahl

Genus Cohnilembus Kahl (Lembus Cohn). Slender spindle-form; peristome from anterior end to the middle of body or longer, curved to right, with 2 membranes on right edge; a caudal cilium or a few longer cilia at posterior end; macro nucleus oval, central; in salt or fresh water, some parasitic.
flexible;

C. fusiformis (C.) (Fig. 328, /). Striation spiral; peristome about 1/6 the body length; a few cilia at posterior end; oval macronucleus central; contractile vacuole posterior; about 60ju long; in fresh water.

C. caeci

Powers

(Fig. 328, g).

About

32-92/z long; in the intestine of

Tripneustes esculentus and other echinoids; Tortugas.

Family 5 Philasteridae Kahl

Genus Philaster Fabre-Domergue

cylindrical; peristome

(Philasterides

Kahl).

Body

about 1/3-2/5 the body length, broader near cytostome and with a series of longer cilia; cytostome with a triangular membrane; cyto pharynx (?); ciliation uniform; a caudal cilium; trichocysts; oval macronucleus with a micro nucleus, central; contractile

vacuole terminal or central; in salt or fresh water.

P. digitiformis F-D. (Fig. 328, h). Anterior region bent dorsally;

contractile vacuole terminal; 100-150^ long; salt water.

772

PROTOZOOLOGY
i).

P. armata (K.) (Fig. 328,

Anterior end more or less straight;

peristome

difficult to see; contractile

vacuole central; 70-80ju long;

fresh water.

Genus Helicostoma Cohn. Similar

to Philaster in general appear-

ance; preoral side-pouch curved around posterior edge of peristome

and separated from it by a refractile curved band; with or without a pigment spot near cytostome; macronucleus oval or band-form;
contractile vacuole terminal; in salt water.

H. buddenbrocki Kahl
brackish water.

(Fig. 328, j).

130-200/* long; in salt and

References

Beers, C. D.: (1933) The ingestion

:

of large amoebae by the ciliate Frontonia leucas. J. El. Mitch. Sc. Soc, 48:223. Bullington, W. E. (1930) A study of spiraling in the ciliate Frontonia with a review of the genus, etc. Arch. Protist., 92:10. Burbank, W. D.: (1942) Physiology of the ciliate Colpidium colpoda. I. Physiol. Zool., 15:342. Corliss, J. O.: (1952) Comparative studies on holotrichous ciliates in the Colpidium-Glaucoma-Leucophrys-Tetrahymena group. I. Tr. Am. Micr. Soc, 71 159. (1952a) Review of the genus Tetrahymena. Proc. Soc. Pro:

toz., 3:3.

Faure-Fremiet,

morphogenetique chez

E.: (1948) Doublets homopolaires et regulation le cilie Leucophrys patula. Arch. d'Anat.

Micr. Morph. Exp., 37:183.

and Mugard, Helene: (1946) Sur un infusoire holotriche histiophage, Deltopylum rhabdoides n. g., n. sp. Bull soc. zool. France., 71:161. (1949) Le dimorphisme de Espejoia mucicola. Hydrobiologia, 1:379. Furgason, W. H.: (1940) The significant cytostomal pattern of the
"Glaucoma-Colpidium group," and a proposed new genus and Tetrahymena geleii. Arch. Protist., 94:224. Gelei, G. v.: (1940) Cinetochilum und sein Neuronemensvstem.
species,
Ibid., 94:57.

Kahl, A.: (1931) Urtiere oder Protozoa. Dahl's Die Tierwelt

Deutschlands,
:

etc.

Part 21.
ciliates.

Kidder, G. W. (1941) Growth studies on

80:50.

VII.

Biol. Bull.,

and Diller, W. F.: (1934) Observations on the binary fission of four species of common free-living ciliates, etc. Ibid., 67: 201. Lilly, D. M. and Claff, C. L.: (1940) Growth studies on ciliates. IV. Ibid., 78:9. Kozloff, E. N.: (1946) The morphology and systematic position of a holotrichous ciliate parasitizing Deroceras agreste. J. Morphol.,
,

79:445.

HOLOTRICHA
Kruger,

773

F.: (1931) Dunkelfelduntersuchungen iiber den Bau der Trichocysten von Frontonia leucas. Arch. Protist., 74:207. Noland, L. E.: (1937) Observations on marine ciliates of the Gulf coast of Florida. Tr. Am. Micr. Soc, 56:160. Parducz, B.: (1939) Korperbau und einige Lebenserscheinungen von Uronema marinum. Arch. Protist., 92:283. (1940) Verwandtschaftliche Beziehungen zwischen den Gattungen Uronema und Cyclidium. Ibid., 93:185. Powers, P. B. A.: (1933) Studies on the ciliates from sea urchins. I. Biol. Bull., 65:106. (1935) Studies on the ciliates of sea-urchins. Papers Tortugas Lab., 29:293. Rossolimo, L. L.: (1926) Parasitische Infusorien aus dem BaikalSee. Arch. Protist., 54:468. Wenrich, D. H.: (1929) Observation on some freshwater ciliates. I. Tr. Am. Micr. Soc, 48:221.

Chapter 36

Order

Holotricha Stein (continued)

Suborder 5 Thigmotricha Chatton and Lwoff

HE
or

majority of the

ciliates

placed in this suborder are parasites

possess thigmotactic cilia with which they attach themselves to the host body. Though appearing heterogeneous, Chatton and Lwoff (1949) maintain that there is a phylogenetic unity among them, which condition has been brought about by degenerative influence because of similar conditions of habitat. Taxonomy (Jarocki and Raabe, 1932; Chatton and Lwoff,
of molluscs.

commensals

They

1949).

Following Chatton and Lwoff (1939), the suborder

into seven families:

is

here divided

Family Family Family Family Family Family Family

Family
1

Conchophthiridae
(p.

2 Thigmophryidae 4 Hysterocinetidae
6

776)
779)

3 Hemispeiridae (p. 776)

(p.

5 Ancistrocomidae (p. 780)

Hypocomidae

(p.

784)

7 Sphenophryidae (p. 785).

Conchophthiridae Reichenow

Genus Conchophthirus Stein. Oval to ellipsoid; flattened; right margin concave at cytostomal region, left margin convex; ventral surface somewhat flattened, dorsal surface convex; cytostome on right side near middle in a depression with an undulating membrane; macro nucleus; micro nucleus; contractile vacuole opens through a canal to right side in the mantle cavity and gills of various mussels. Species (Kidder, 1934, 1934a; Uyemura, 1934, 1935); morphology
;

(Raabe, 1932, 1934; Kidder, 1934). C. anodontae (Ehrenberg) (Fig. 329, a). Ovoid; cytostome in anterior third, with an overhanging projection in front; cytopharynx, surrounded by circular fibrils, continues down as a fine, distensible tubule, to near the macronucleus; with peristomal basket; ciliary grooves originate in a wide ventral suture near anterior end; anterior region filled with refractile granules; macronucleus
posterior; contractile vacuole

slit-like

aperture (Fig. 27); 65-125/*

cavity, gills

between nuclei and peristome, with by 47-86^; in the mantle and on non-ciliated surface of palps of Elliptio comHole.
774

planatus;

Woods

HOLOTRICHA

775

Myxophyllum

magna, X300 (Kidder); c, Hemispeira asteriasi, X705 (Wallengren) e, f Protophrya ovicola (Cepede) (f a young Littorina rudis with the ciliate); g, h, two views of Ancistruma mytili, X500 (Kidder); i, A. isseli, X500 (Kidder); j, A. japonica, X600 (Uyemura); k, Eupoterion
Fig. 329.
a,

Concophthirus anodontae;
,

b, C.
;

steenstrupi,

X280 (Raabe)

d,

pernix,

X500 (MacLennan and

(Fig. 329, b).

Connell);

1,

Ancistrina ovata,

X630

(Cheissin).

C.

magna Kidder

Much larger;

123-204/i

by 63-116/*;

closer ciliation; anterior 1/3 filled with smaller granules; irregularly

outlined macronucleus, 25-30m in diameter, central; 2 (or 1) micronuclei; aperture for contractile vacuole large; mantle cavity of Elliptic)

complanatus; Massachusetts.

776
C. mytili de

PROTOZOOLOGY
Morgan
(Fig. 56).

Reniform; 130-220/* by 76-161/x;

peristomal groove on the right side; trichocysts conspicuous along

frontal margin; macronucleus oval; 2 micronuclei; on the foot of the

common
1933b,

mussel, Mytilus edulis. Division and conjugation (Kidder,

c).

flexible ;

Genus Myxophyllum Raabe. Oval or spheroid; pellicle elastic and peristome on posterior right, without undulating membrane;
;

7 macronuclei; a micronucleus ciliation uniform; in the slime cover-

ing land pulmonates.

M.

steenstrupi (Stein) (Fig. 329,

c). 120/i

by

100-120/*;

on Succinea

putris, etc.

Family 2 Thigmophryidae Chatton and Lwoff

Genus Thigmophrya Chatton and Lwoff. Elongate round or oblong

;

cytostome in posterior third; contractile vacuole opens in cy to pharynx; on the gills or palps of lamellibranchs. T. macomae C. and L. Elongate ovoid; flattened; ventral surface slightly concave; oral funnel opened; contractile vacuole opens at the bottom of cytopharynx; numerous ciliary rows; about 110m by 40m; on the gills of Macoma (TelUna) balthica (Chatton and Lwoff,
in cross section;

1923).

Family 3 Hemispeiridae Konig

Genus Hemispeira Fabre-Domergue (Hemispeiropsis Konig).

Nearly spherical; flattened; longitudinal non-ciliated furrow on ventral surface, which encircles thigmotactic posterior cilia; 4-5 crossfurrows of cilia a huge adoral membrane at anterior end macronucleus, micronucleus large; contractile vacuole, anterior-right; com:

mensal.

H.

asteriasi

F.-D

(Fig. 329, d). 20-30/x long;

ectocommensal on

Asterias glacialis (Wallengren, 1895).

Genus Protophrya Kofoid

(Isselina Cepede). Ellipsoid to pyriform;

spherical macronucleus; cytostome close to the posterior end.

Taxon-

(Raabe, 1949); ciliation (Chatton and Lwoff, 1949). P. ovicola K. (Fig. 329, e, /). About 60m long; in the uterus and brood-sac of the molluscs, Littorina rudis and L. obtusata (Kofoid,
1903).

omy

Genus Ancistruma Strand (Ancistrum Maupas). Ovoid, pyriform

or somewhat irregular; flattened; right side with more numerous
large cilia than the left; peristome

on right

side;

cytostome near

posterior extremity; macronucleus round or sausage-shape, central;

a micronucleus; contractile vacuole posterior; commensal in the

mantle cavity of various marine mussels.

reproduction (Kidder, 1933, 1933a).

Many species. Morphology,

HOLOTRICHA

777

A. my tili (Quennerstedt) (Figs. 18; 329, g, h). Oval; dorsal surface convex, ventral surface concave; dorsal edge of peristome curves around the cytostome; peristomal floor folded and protruding; longitudinal ciliary rows on both surfaces; three rows of long cilia on peristomal edges; macro nucleus sausage-form; a compact micronucleus anterior; 52-74ju by 20-38/z. Kidder (1933) found it in abundance in the mantle cavity of Mytilus edulis at Woods Hole and New York.
(Fig. 329, *). Bluntly pointed at both ends; 70-88/x Kidder (1933) observed it abundantly in the mantle cavity of the solitary mussel, Modiolus modiolus, Massachusetts and New York, and studied its conjugation and nuclear reorganization.

A.

isseli

Kahl

by

31-54ju.

A. japonica Uyemura (Fig. 329, j). Body oval or elongate pyriform; 55-76(67) /z by 14-29(20) n; subspherical macronucleus conspicuous; a compact micronucleus; usually a single contractile vacuole, posterior; in the mantle cavity of marine mussels; Meritrix meritrix, Paphia philippinarum, Cyclina sinensis, Mactra veneriformis, M. sulcataria, and Dosinia bilnulata (Uyemura, 1937).

Genus Eupoterion MacLennan and Connell. Small ovoid slightly compressed; cilia short, in longitudinal rows; rows of long cilia in peristome on mid-ventral surface and extend posteriorly, making a half turn to left around cytostome; small conical cytostome lies in postero -ventral margin of body; contractile vacuole terminal; large round macronucleus anterior; a micronucleus; commensal.
;

E. pernix M. and C. (Fig. 329, k). 46-48 ciliary rows; 6 rows of heavy peristomal cilia; 38-56/x long; in the intestinal contents of the

mask limpet, Acmaea persona; California. Genus Ancistrina Cheissin. Ovoid; anterior end attenuated;
stomal
field

peri-

along narrow right side; 15-18 ciliary rows parallel to

peristomal ridges; cytostome right-posterior, marked with oral ring, with a membrane and a zone of membranellae right ridge of peristome marked by two adoral ciliary rows; macronucleus anterior, spheroidal; a micronucleus; commensal.
;

A. ovata C. (Fig. 329, 1). 38-48/x by 15-20/*; in the mantle cavity of molluscs: Benedictia biacalensis, B. limneoides and Choanomphalus
sp.

Genus Cochliophilus

Kozloff.

Ovoid and compressed; peristome

in

right-posterior fourth of the body; membrane-like fine cilia overlie a

series of thick cilia from the anterior end of the peristome to cytostome; longitudinal rows of cilia; a vesicular micronucleus; an ovoid macronucleus; a contractile vacuole; in molluscs.

C. depressus

K.

(Fig. 330, a).

About

93/z

by 63m by 15m; 52-56

778
ciliary rows; peristomal

PROTOZOOLOGY
membraneous
cilia

motile; macronucleus obsnail,

long; in the mantle cavity of the

pulmonate

Phytia

setijer in

San Francisco Bay (Kozloff, 1945). Genus Ancistrella Cheissin. Elongate; ends rounded; ventral
ciliation uniform, except anterior-dorsal region,

sur-

face less convex than dorsal surface; 16-17 longitudinal ciliary rows;

bearing bristle-like

longer
sally

cilia;

2 adoral ciliary rows on right of peristome, curved dor-

single or divided into as

behind cytostome; contractile vacuole posterior; macronucleus many as 7 parts; micronucleus; commensal. A. choanomphali C. (Fig. 330, b). 55-90ju by 18-20/u; in the mantle

cavity of Choanomphalus sp.

Fig. 330.

a,

Cochliophilus depressus,

X600

(Kozloff); b, Ancistrella

choanomphali, X840 (Cheissin); c, Boveria teredinidi, X550 (Pickard); d, Plagiospira crinita, X740 (Issel); e, Hysterocineta eiseniae, X250 (Beers); f, Ptychostomum bacteriophilum X500 (Miyashita).
,

HOLOTRICHA

779

Genus Ancistrospira Chatton and Lwoff. Ciliation meridional to spiral; peristome right spiral; commensal.
A. veneris C. and L. 50-60/z by 22-28^; ovoid, anterior end
pointed; ciliary rows meridional; thigmotactic field on the
left side,

sharply marked from body ciliation; on the

gills

of Venus fasciata.

Genus Boveria Stevens

(Tiarella Cheissin). Conical; cytostome

at posterior end; peristome spiral posteriorly; macronucleus oval,

in anterior half; a micronucleus; contractile vacuole posterior; ecto-

commensal on gills of various marine animals such as Teredo, Bankia, Tellina, Capsa and Holothuria. Several species. B. teredinidi Pickard (Fig. 330, c). 27-173/i by 12-3 1m; on gills of
Teredo navalis; California (Pickard, 1927).

Genus Plagiospira Issel. Conical; anterior end attenuated; peristome runs spirally from middle of body to cytostome, with long
ole near middle of

marcronucleus oval, anterior; a micronucleus; contractile vacubody; somewhat spirally arranged striae widely apart on right side; commensal.
cilia
;

P. crinita

I.

(Fig. 330, d). 32-58ju

by 18-34^;

in Cardita calyculata

and Loripes

lacteus.

Family 4 Hysterocinetidae Diesing

Inclusion of this family in the present suborder
its affinity
it

is

provisional, since

to other forms
in

is

not yet

clear.

Beers (1938)

who

placed

agreement with Cheissin (1931), states that the nutrition is in part saprozoic, and that the organisms are in the process of acquiring the saprozoic and astomatous condition.
in

Hymenostomata,

Genus Hysterocineta Diesing (Ladopsis Cheissen). Elongate;

flattened; flexible,

an inverted V- or U-shaped sucker conspicuously

present in antero- ventral margin; ciliation uniform; cytostome and

cytopharynx at the posterior end; an undulating membrane along peristome which borders the posterior margin of body; macronucleus
elongate; a micronucleus; contractile vacuole posterior; in the intestine of gastropods

and oligochaetes. 4

species.

Taxonomy

(Jarocki,

1934; Beers, 1938; Raabe, 1949).

H. eiseniae Beers

(Fig. 330, e). 190-210/x

by

35-40/x; cytostome

not functional; endoplasm with small granules; macronucleus 45-50^

long; sucker inverted V, about 25-30;u long; in the intestine of Eisenia lonnbergi (Beers, 1938).

Genus Ptychostomum
Several species.

Stein (Lada Vejdovsky). Sucker circular or

ovoid; macronucleus ovoid or reniform, not elongate; in oligochaetes.

Taxonomy

(Studitsky, 1932; Raabe, 1949).

780

PROTOZOOLOGY

by

P. bacteriophilum Miyashita (Fig. 330,/). Elongate oval; 70-130/* 30-45/*; sucker oval and large, about 50/* in diameter; macronu-

cleus ellipsoid;

endoplasm with numerous rods (symbiotic bacteria?)

in the freshwater oligochaete, Criodrilus sp.

Family 5 Ancistrocomidae Chatton and Lwoff

Genus Ancistrocoma C. and L. (Parachaenia Kofoid and Bush). Elongate pyriform with attenuated anterior end; somewhat flattened dorso-ventrally; a contractile suctorial tentacle at the anterior tip, which is used for attachment to the epithelium of host, and which continues internally as a long curved canal; longitudinal ciliation on dorso-lateral and ventral sides, beginning at the anterior
end; parasitic in the
gills

and palps

of mollusks.

Taxonomy

(Kozloff,

1946b; Chatton and Lwoff, 1950). A. pelseneeri C. and L. (Parachaenia myae Kofoid and Bush) (Fig.
331, a).

Body

50-83(62)/*

by

14-20(16)/*

by 11-16(12.5) a*; 14

ciliary

rows on dorso-lateral and ventral surfaces; five rows on the ventral side extend only 2/3 from the anterior end; tentacle continues internally for about 2/3 of body, curved; macronucleus sausageshaped; a single micronucleus; on the gills and palps of mussels:

Mya
mya

arenaria,

M.

irus,

M.

inconspicua,

M.

nasuta,

M.

secta,

Crypto-

californica (Kozloff, 1946b).

Genus Hypocomagalma Jarocki and Raabe. Ovoid or pyriform with attenuated anterior end; asymmetrical; 22-24 ciliary rows which do not reach the posterior end; a suctorial tentacle at the anterior end; on mollusks.
H. pholadidis Kozloff
tractile vacuoles;

(Fig. 331, b). 63-89/*

by

18-25/*

anterior end bent ventrally; 24 or 25 ciliary rows; one or

cleus; parasitic in the epithelium of the gills

by 16-21/*; more con-

macronucleus sausage-shaped; a single micronuand palps of Pholadidea

Collin.

penita (Kozloff, 1946b).

Elongate ovoid, narrowed anteend; 14 ciliary rows (six dorsal, six ventral and two lateral) on molluscs (Collin, 1914). S. pterotrachae C. Body 55/* by 25/*; macronucleus elongate band; on the gills of Pterotracha coronata (Chatton and Lwoff, 1950). Genus Goniocoma Chatton and Lwoff. Ovoid with attenuated anterior end; end of suctorial tentacle extremely slender; 27-29 ciliary

Genus Syringopharynx

riorly; a suctorial tentacle at anterior

;

is very short and the rows on either side of it are progressively longer; ventral rows pass over the posterior end and terminate on dorsal surface; on the gills

rows; of the 14 dorsal rows, the median row

of molluscs.

HOLOTRICHA

781

Fig. 331, a, ventral view of a stained Ancislrocoma pelseneeri, X1120 (Kozloff); b, Hypocomagalma pholadidis, X840 (Kozloff); c, ciliature as

viewed from right side of Holocoma primigenius, X1130 (Chatton and Lwoff) d, ventral view of Insignicoma venusta, X1245; e, Raabella botulae, XI 245; f, Crebricoma kozloffi, X755 (Kozloff).
;

G. macomae (C. and L.). Body 33-39^ by 13-18/*; a comparatively voluminous micronucleus; on the gills and palps of Macoma balthica (Chatton and Lwoff, 1950). Genus Holocoma Chatton and Lwoff. Cylindrical; ventral surface convex; tentacle at anterior end; 19-23 ciliary rows; 6-10 median dorsal rows relatively short, seven left and six right rows long on the
;

gills of

mollusks.
(Fig. 331, c).

H. primigenius C. and L.

Elongated body 41-59m

gills

by 15^; ventral
of

surface convex; elongate macronucleus; on the

Macoma

balthica

(Chatton and Lwoff, 1950).

782

PROTOZOOLOGY
Kozloff. Elongate pyriform; a contractile ten-

Genus Insignicoma
of ventral surface;
set;

tacle with internal canalicule;

median

ciliary

rows on anterior half

and closely an inverted V-shaped row of long cilia on left-lateral surface at about the middle of body; on mollusks. /. venusta K. (Fig. 331, d). 42-52/* by 18-21/1 by 15-18/z; 15 median, two right, and 16-17 left ciliary rows; macronucleus ovoid; micronucleus spherical; on the gills and palps of Botula californiensis
right ciliary rows; left rows short
(Kozloff, 1946a).

two

Genus Raabella Chatton and Lwoff. Three groups of ciliary rows; median rows; six to 11 longer rows on left-lateral side; two longer rows on the right side; on mollusks. R. botulae (Kozloff) (Fig. 331, e). 31-39/* by 14-17/x by 12-14/x; 11 median rows; 11 closely set left rows; two longer right rows; macroeight to 11 short

nucleus ovoid to sausage-shaped; spherical micronucleus; on the

gills

and palps of Botula californiensis (Kozloff, 1946a). Genus Crebricoma Kozloff. Pyriform; anterior suctorial
ciliary rows, the

tentacle;

many

majority of which are closely set; two long rows on the right side; anterior terminals of the rows make a V-

shaped suture; on the

C. kozloffi

gills of

mollusks.

Chatton and Lwoff (C. carinata K.) (Fig. 331, /). Body 58-71// by 27-39/x by 22-3 l/i; two ciliary rows on right side long, about 2/3 the body length; more than 30 rows of closely set cilia (1/2-2/3 the body length and longer toward left); macronucleus ellipsoid; on the gills and palps of Mytilus edulis (Kozloff, 1946; Chatton and Lwoff, 1950).

Genus Hypocomides Chatton and Lwoff. Elongate; some 23

short curved

cili-

ary rows; about 20 median rows, short; two longer rows on right; a

row near the posterior end; on mollusks. H. mediolariae C. and L. (Fig. 332, a). 27-50/t by 15-27/*; on the gills of Mediolaria marmorata (Chatton and Lwoff, 1922).
flattened; 12 ciliary rows;

Genus Anisocomides Chatton and Lwoff. Body ovoid, slightly two short median rows with five additional

rows which are progressively longer toward left; a short oblique row, posterior to the outermost left row; four right rows much longer; on
the
gills of

mollusks.
;

A. zyrpheae (C. and L.) (Fig. 332, b). 19-38 M by 10-1 5/x by 7-10 M on the gills of Pholas (Zyrphea) crispata (Chatton and Lwoff, 1926).
comides, but without the short posterior ciliary row; on the

Genus Hypocomatidium Jarocki and Raabe. Similar to Anisogills of

mollusks.

783

Fig. 332, a, Hypocomides mediolariae, X1000; b, left side view of Anisocomides zyrpheae in life, X1065; c, Isocomides mytili in life, X1000 (Chatton and Lwoff); d, Hypocomina tegularum, X1245; e, Heterocinetopsis goniobasidis, XI 145; f-h, Hypocomella phoronopsidis, X1300 (f, ventral view of a stained specimen; g, h, dorsal and right side views in life) i, Enerthecoma kozloffi,, X1145 (Kozloff).
;

and R. Ovoid; 30-45/x by 14-18/u by 9-12^; nine rows on left- ventral and four on right; on the gills of Sphaerium corneum and S. rivicola (Jarocki and Raabe, 1932). Genus Isocomides Chatton and Lwoff. Elongated; 14-18 ciliary rows on anterior 2/3 of the ventral surface six to seven on right and eight to 11 on left; in addition, there is a short transverse row with a dozen long cilia, posterior to other rows; on mussels. /. mytili (C. and L.) (Fig. 332, c). 57-64 M by 20-22 M on the gills of Mytilus edulis (Chatton and Lwoff, 1922). Genus Hypocomina Chatton and Lwoff. Ovoid to pyriform; an
H.
stphaerii J.

ciliary rows; five

784

PROTOZOOLOGY
little

anterior tentacle; eight to 10 ciliary rows about half the body-length

and starting a
lusks.

distance

away from the

anterior tip; on mol-

H. tegularum Kozloff

(Fig. 332, d). 26-36/x

by

12-17/u

by

9-12/z;

anterior end bent ventrally; nine ciliary rows, five rows on right be-

ing slightly longer than the other four; spherical macronucleus; parasitic

on the ctenidium

of Tegula

brunnae (Kozloff, 1946).

Genus Heterocinetopsis

Jarocki.

Body

elongate, flattened dorso-

ventrally; a contractile tentacle, its canalicule extending 1/3-2/3

the body length; 10-12 ciliary rows; the median rows about one-half the body length, the rows toward left being progressively longer; on

mollusks (Jarocki, 1935).

H. goniobasidis (Kozloff)
14:11)

(Fig. 332, e). 36-48/x

by
gills

15-20/*

by 11of

10 ciliary rows; macronucleus pyriform; ovoid micronucleus

inconspicuous; parasitic on the epithelium of the

Goniobasis plicifera silicula (Kozloff, 1946c).

and mantle

Genus Hypocomella Chatton and Lwoff (Hypocomidium Raabe). Pyriform, asymmetrical, flattened; a long retractile tentacle; seven
to 13 ciliary rows on the ventral surface, three rows on left being

progressively longer; on mollusks (Chatton

H. phoronopsidis (Kozloff)
6.5-1 1/x; eight ventral ciliary

(Fig. 332, f-h). 26-37/:

and Lwoff, 1922, 1950). by 11-16/* by rows; ovoid macronucleus and micro-

nucleus; on the tentacles of Phoronopsis viridis (Kozloff, 1945a).

Genus Enerthecoma
rows on the ventral
five others

Jarocki. Pyriform, symmetrical; 8 ciliary

on left are somewhat separated from and closely set; on the gills of mollusks. E. kozloffi Chatton and Lwoff (Fig. 332, i). 32-56/z by 13-21 n by 10-13/*; eight ciliary rows about 2/3 the body length; macronucleus elongate micronucleus fusiform on the gills of Viviparus fasciatus and V. malleatus (Kozloff, 1946c; Chatton and Lwoff, 1950). Genus Cepedella Poyarkoff Pyriform with a pointed anterior end
side; three
;

macronucleus globular; without contractile vacuole.

C. hepatica P.

Body

16-26/x long; in the liver of

Sphaerium

cor-

neum.

Family 6 Hypocomidae Butschli

Griiber. Dorsal side convex; ventral side flattened with a ciliated oval field; a suctorial tentacle at the anterior end; about 13 ciliary rows; an adoral zone, a short row (eight granules) at anterior-left side;

Genus Hypocoma

on colonial Protozoa. H. parasitica G. (Fig. 333, a). 30-38/x by 18-20/x by 18/t; 13 ciliary rows on the flattened surface: adoral zone, a short row; 11 general

HOLOTRICHA
ciliary rows;

785

macronucleus horseshoe-shape; a large central food vacuole; on solitary or colonial peritrichs such as Vorticella, Zoothamnium, etc. (Chatton and Lwoff, 1950). Genus Heterocoma Chatton and Lwoff. Body ovoid; ventral side flattened; suctorial tentacle antero-ventral 13 ciliary rows make an ellipsoidal field; an adoral zone, five closely-set rows on left and
;

Fig. 333.

a,

Hypocoma

X1200;
in life

c,

ciliature of

parasitica, X1350; b, Heterocoma hyper parasitica, Parahypocoma collini, as seen from left-ventral side

(Chatton and Lwoff).

seven widely separated rows on right; in the branchial cavity of

Salpa (Chatton and Lwoff, 1939).

H. hyperparasitica C. and L.
in
;

(Fig. 333,

b).

Body

ovoid, with

bluntly pointed posterior end; about 44 p. long; a large food vacuole

cytoplasm in the branchial cavity of Salpa mucronata-democratica (Chatton and Lwoff, 1950). Genus Parahypocoma Chatton and Lwoff. Ellipsoid; highly flattened; anterior end tapers slightly; 29-34 ciliary rows; the adoral
zone as in the other two genera; a comparatively short suctorial tentacle at anterior end; macronucleus horseshoe-shaped; a large cen-

tral

food vacuole; parasitic in ascidians.

c). In Ascidia mentula and Ciona (Chatton and Lwoff, 1950).

P. collini C. and L. (Fig. 333,

intestinalis

Family 7 Sphenophryidae Chatton and Lwoff

Genus Sphenophrya Chatton and Lwoff. Body elongated, "quarter orange-" or

banana-shaped; attached to the

gills of

host mollusks

786

PROTOZOOLOGY
suctorial tentacle; adult stage without cilia; ciliature
is

by a

reduced

by budding; embryos are ciliated; on the gills of mollusks (Chatton and Lwoff, 1921). S. dosiniae C. and L. (Fig. 334, a-c). Body 120ju by 15-2(V; young embryo ciliated on the gills of Dosinia exoleta, Venus ovata, Corbula gibba, etc. (France) Mactra solidissima (Woods Hole) (Chatton and
to infraciliature of 2 groups; multiplication
;
;

Lwoff, 1950).

Fig. 334, a-c, Sphaenophrya dosiniae (a, a young embryo; b, a growingindividual attached to an epithelial cell of the host by a suctorial tentacle; c, an individual from which a bud is ready to separate) d, a side view of
;

Pelecyophrya tapetis in life; e, f, Gargarius gargarius, XI 200 (e, in life, showing a macronucleus and a micronucleus; f, diagram showing the
ciliature)

(Chatton and Lwoff).

Genus Pelecyophrya Chatton and Lwoff. Body hatchet-shaped,

laterally compressed; posterior

anterior end; infraciliature in

left;

end rounded; a large "sucker" at the two groups, five on right and four on multiplication by budding; on the gills of mollusks (Chatton and

Lwoff, 1922). P. tapetis C. and L. (Fig. 334, d). Body 23-25/x by about 10 ; macronucleus spherical; ovoid micronucleus; cytoplasm contains

HOLOTRICHA
including nuclei; conjugation; on the

787
gills of

fragments of host cells Tapes aureus (Chatton and Lwoff, 1950). Genus Gargarius Chatton and Lwoff. Dorso-ventrally flattened; with a "horn" near the anterior end; sucker occupies the entire ventral surface, its margin showing papillous extensions; on the ventral surface there are two groups of ciliature; four rows on each side; on

Mytilus (Chatton and Lwoff, 1934).

G. gargarius C. and L. (Fig. 334, e, /). Body about 35m long; ciliated embryos formed by budding or unequal division; macronucleus elongate; micronucleus spherical; on Mytilus edulis (Chatton and

Lwoff, 1950).

References

Beers, C. D.: (1938) Hysterocineta

516.

eiseniae, etc. Arch. Protist., 91:

Chatton, E. and Lwoff, A.: (1922) Sur

1'evolution des infusoires des lamellibranches, etc. C. R. Acad. Sc, 175:787. (1923) Sur revolution des infusoires des lamellibranches. Ibid., 177:81. (1926) Diagnoses de cilies thigmotriches nouveaux. Bull. Soc.Zool.Fr., 51:345. (1939) Sur le sucoir des infusoires thigmotriches rhyncoides, etc. C. R. Acad. Sc, 209:333. (1949) Recherches sur les cilies thigmotrichs. I. Arch. zool. exper. gen., 86:169. (1950) II. Ibid., 86:393. Cheissin, E.: (1931) Infusorien Ancistridae und Boveriidae aus dem Baikalsee. Arch. Protist., 73:280.

Jarocki,

J.:

(1934)

nickii, etc.

Two new hypocomid ciliates. Heterocineta jaMem. Acad. Pol. Sci. Lett. CI. Math. Nat. Ser. B,

Sc. Nat., p. 167.

and Raabe, Z.: (1932) Ueber drei neue Infusorien-Genera der Familie Hvpocomidae, etc. Bull. Acad. Pol. Sc. Lett. Ser. B. Sci. Nat. (II), p. 29. Kidder, G. W.: (1933) On the genus Ancistruma. I. Biol. Bull, 64:
1.

(1933a) II. Arch. Protist., 81:1. Ibid., 79: 1. (1933b) Studies on Conchophthirius mytili. I. (1933c) II. Ibid., 79:25. (1933d) Conchophthirius caryoclada sp. nov. Biol. Bull., 65:
175.

(1934) Studies on the ciliates from freshwater mussels.

Ibid., 66:69.

I.

(1934a)

II. Ibid.,

66:286.
kais.

Konig, A.: (1894) Hemispeiropsis comatulae, etc. Sitzb. Wiss., Wien. M.-N. CI., 103:55. Kofoid, C. A.: (1903) On the structure of Protophrya Mark Anniv. Vol., Harvard Uni., p. 111.

Akad.

ovicola, etc.

788

PROTOZOOLOGY
of

and Bush, Mildred: (1936) The life cycle etc. Bull. Mus. Roy. Hist. Nat., 12:1. Kozloff, E. N.: (1945) Cochliophilus depressus, etc.
myae,
95.

Parachaenia

Biol. Bull., 89:

Ibid., 89:180. (1945a) Heterocineta phoronopsidis, etc. (1946) Studies on ciliates of the family Ancistrocomidae, Ibid., 90:1. etc. I. (1946a) II. Ibid., 90:200. (1946b) III. Ibid., 91:189. (1946c) IV. Ibid., 91:200. MacLennan, R. F. and Connell, F. H.: (1931) The morphology of Eupoterion pernix. Univ. California Publ. Zool., 36:141. Miyashita, Y. (1933) Drei neue parasitische Infusorien aus dem Darme einer japanischen Susswasseroligochaete. Ann. Zool. Japon., 14:127. Mjassnikowa, Marie: (1930) Sphenophrya sphaerii, etc. Arch. Protist., 71:255. Pickard, Edith A.: (1927) The neuromotor apparatus of Boveria teredinidi, etc. Univ. California Publ. Zool., 29:405. Raabe, Z.: (1934) Weitere Untersuchungen an einigen Arten des Genus Conchophthirus. Mem. Acad. Pol. Sc. Lett. Ser. B, 10:
:

221. (1949) Recherches sur les cilies thigmotriches. III. Ann. Univ. Marie Curie-Ski. Sec. C, 4:119. Stevens, N. M.: (1903) Further studies on the ciliate Infusoria, Licnophora and Boveria. Arch. Protist., 3:1. Studitsky, A. N.: (1932) Ueber die Morphologie, Cytologic und

Systematik von Ptychostomum

chattoni. Ibid., 76:188.

Uyemura, M.:

(1934) Ueber einige neue Ciliaten aus dem Darmkanal von japanischen Echinoidien. I. Sc. Rep. Tokio Bunrika Daigaku, 1:181. (1935) Ueber drei in der Susswassermuschel lebende Ciliaten (Conchophthirius). Ibid., 2:89. (1937) Studies on ciliates from marine mussels in Japan. I. Ibid., 3:115. Wallengren, H.: (1895) Studier ofver ciliata infusorier. II. 77 pp.

Lund.

Chapter 37

Order

Holotricha Stein (continued)

Suborder 6 Apostomea Chatton and Lwoff

ASYMMETRICAL forms with a rosette-like cytostome through

which liquid or small
solid particles are

taken into the body;

sparse ciliary rows spiral; adoral rows short; macronucleus oval to

band-form; a micro nucleus; a single contractile vacuole. The life-cycle of the ciliates grouped here appears to be highly complex and Chatton and Lwoff (1935) distinguished several developmental phases (Fig. 335), as follows: (1) Trophont or vegetative
phase: right-spiral ciliary rows; nucleus pushed aside by food bodies; body grows, but does not divide. (2) Protomont transitory stage between 1 and 3 in which the organism does not nourish itself, but pro:

duces "vitelloid" reserve plates; nucleus central, condensed ciliary rows become straight. (3) Tomont: the body undergoes division usually in encysted condition into more or less a large number of
;

small ciliated individuals. (4) Protomite a stage in which a renewed torsion begins, and which leads to tomite stage. (5) Tomite: small
:

free-swimming and non-feeding stage, but serves for distribution. (6) Phoront: a stage which is produced by a tomite when it becomes attached to a crustacean and encysts; within the cyst a complete transformation to trophont takes place.

Family Foettingeriidae Chatton

Genus Foettingeria Caullery and Mesnil. Trophonts large, up to 1 mm. long; sublenticular, anterior end attenuated; dorsal surface conthan left side; 9 rows nearly evenly arranged; in gastro vascular cavity of various actinozoans; tomont on outer surface of host body, gives rise to numerous to mites with meridional ciliary rows; each tomite becomes a phoront by encysting on a crustacean, and develops into a trophont when taken into gastrovascular cavity of an actinozoan.
vex, ventral surface concave; right side less convex
spiral ciliary

One

species.

F. actiniarum (Claparede) (Fig. 336, a). Phoronts

on Copepoda,

Ostracoda, Amphipoda, Isopoda and Decapoda; trophonts in Actinia mesembryanthemum, A. equina, Anemonia sulcata and other
actinozoans in European waters; Chatton and Lwoff found Metridium marginatum, Sagartia leucolena and Astrangia danae of Woods Hole free from this ciliate. Genus Spirophrya Chatton and Lwoff. Trophonts ovoid, pointed anteriorly; 16 uninterrupted ciliary rows of which striae 1 and 2 ap789

790

PROTOZOOLOGY
(Idyaea furcata)

Young trophont
Phoront:

Fig. 335.

Diagram

illustrating the life-cycle of Spirophrya

subparasitica (Chatton

and Lwoff).

proach each other in posterior-dorsal region; phoronts attached to a crustacean; when eaten by Cladonema, trophonts enter the crustacean body and complete growth; protomonts upon leaving the host body encyst and each divides into 4-82 tomites (Fig. 335). One
species.

S. subparasitica C.

and

L. (Figs. 335; 336, b).

to Idyaea furcata; ovoid trophonts enter the

Phoronts attached copepod when eaten by

Cladnema radiatum.

HOLOTRICHA

791

Genus Gymnodinioides Minkiewicz (Physophaga Percy; Oospira Chatton and Lwoff). Trophonts twisted along equatorial plane; generally 9 ciliary rows, in some a ruclimentar}^ row between striae 5 and
6 at anterior end.
G. calkinsi
in the

Many species.
;

gills and trophonts moult of Palaemonetes sp. Woods Hole. Genus Phoretrophrya Chatton and Lwoff. Trophonts generally with 9 ciliary rows; striae 1, 2, and 3, close to one another. One spe-

Chatton and Lwoff. Phoronts on

cies.

sitica,

Fig. 336. a, Foettingeria actiniarum, a trophont; b,Spirophrya subparaa trophont, XlOOO; c, Phoretrophyra nebaliae, X1180; d, Synophrya hypertrophica (Chatton and Lwoff).

792

PROTOZOOLOGY
c).

P. nebaliae C. and L. (Fig. 336,

Phoronts and tomonts on ap-

pendages, and trophonts in the moult, of Nebalia geoffroyi.

Genus Synophrya Chatton and Lwoff. Trophonts and tomonts

Fig. 337, a, Ophiurespira weilli; b, Photorophrya insidiosa, a trophont in a phoront of Gymnodinioides, X800; c, Vampyrophrya pelagica, a trophont, X740; d, Pericaryon cesticola, a trophont (Chatton and Lwoff).

similar to those of Gymnodinioides; but

development highly compli-

cated.

One

species.

S. hypertrophica G.

lamellae,

and L. (Fig. 336, d). Phoronts in branchial and trophonts in the moult, of Portunus depurator, etc.

HOLOTRICHA

793

Fig. 338.

a,

Polyspira delagei;

b,

Calospira minkiewiczi, a trophont,

X1300; c, Vampyrophrya pelagica, (Chatton and Lwoff).

d,

Traumatiophtora punctata, X1300

ciliary rows; striae

Genus Ophiurespira Chatton and Lwoff. Trophonts ovoid; 10 9 and 10 interrupted. One species. 0. weilli C. and L. (Fig. 337, a). Trophonts in the intestine of Ophiothrix fragilis and Amphiura squamata (Ophiuroidea). Genus Photorophrya Chatton and Lwoff. Trophonts small ciliation approximately that of Ophiurespira; massive macro nucleus; with
;

peculiar trichocysts comparable with the nematocysts of Polykrikos (p. 324) ecto- or endo -parasitic in encysted stages of other aposto;

means. Several species.

794

PROTOZOOLOGY
b).

P. insidiosa C. and L. (Fig. 337,

Phoronts, trophonts and

tomites in phoronts of Gymnodinioides. Genus Polyspira Minkiewicz. Trophonts reniform; 9 rows and several extra rows; striae 1-4 and 5-9 with 2 others in 2 bands.
P. delagei M. (Fig. 338, a). Phoronts on gills and trophonts in the moult of Eupagurus berhardus. Genus Pericaryon Chatton. Trophonts ellipsoid; 14 ciliary rows. P. cesticola C. (Fig. 337, d). Trophonts in the gastro vascular cavity of the ctenophore, Cestus veneris; other stages unknown. Genus Calospira Chatton and Lwoff. Trophonts resemble those of Spirophrya; 20 ciliary rows; macro nucleus twisted band-form; a
micronucleus.
C. minkiewiczi C. and L. (Fig. 338, b). Phoronts attached to integument of Harpacticus gracilis (copepod); trophonts in its fresh carcass; tomonts and tomites in water. Genus Vampyrophrya Chatton and Lwoff. Trophonts ovoid; 10
ciliary rows.

One

species.
c;

V. pelagica C. and L. (Fig. 337,

fresh carcasses.

338,

c).

nus parvus, Clausocalanus furcatus,

etc.,

Phoronts on Paracalaand trophonts in their

11

ciliary rows.

Genus Traumatiophtora Chatton and Lwoff. Trophonts oval; One species. T. punctata C. and L. (Fig. 338, d). Trophonts in fresh carcass

of

Acartia clausi.

Genus Hyalospira Miyashita. Trophonts in the moult of a freshwater crustacean, with a contractile vacuole and a long accessory canal, and with a band-shaped macro nucleus; protomont encysts in narrow crevices; tomont divides into 2-16 tomites; tomite with a
tubular macronucleus, two ciliated grooves on ventral side, and 9 ciliary rows; phoront cysts occur on the body hairs of Xiphocaridina
to

metamorphose into trophont (Miyashita, 1933). H. caridinae M. (Fig. 339 a). Fully grown trophonts 80-120^ long; phoronts and phoront cysts present in fresh moults and body hairs
respectively of the freshwater shrimp, Xiphocaridina compressa.

Genus Cyrtocaryum Faure-Fremiet and Mugard. Trophont, astomous; external appearance resembles Anoplophrya (p. 691); macronucleus reticulate as in Foettingeria; liberated in sea water; no encystment, but multiplication in free state; differentiation of an oral
ciliary field.

C. halosydnae F. and M. (Fig. 339, b-e). Trophont in the lateral caeca of the digestive tube of Halosydna gelatinosa; pyriform, 90120/x

by 65-80 /x with about 60

;

slightly spiral ciliary rows; cilia in

HOLOTRICHA

795

Fig. 339. a, a newly excysted trophont of Hyalospira caridinae, X1000 (Miyashita); b-e, Cryptocaryum halosydnae (Faur6-Fremiet and Mugard) (b, the infraciliature of trophont, X450; c, tomont of third or fourth generation; d, anterior end view; e, tomite in life, X800).

the anterior region strongly thygmotactic.

spherical individuals in chain, takes place.

When

freed in the sea

water, no encystment occurs, but division into eight to 16 sub-

Tomont 45^

long; to-

mites 20m by

16/x,

asymmetrical, with a long caudal

bristle.

References

Chatton, E. and Lwoff, A.: (1935) Les

zool. exper. gen., 77:1.

cilies

apostomes. Arch-

Faure-Fremiet, E. and Mugard, Helene: (1949) Un infusoire apostome parasite d'un polychete: etc. C. R. Acad. Sc, 228:
1753.

Miyashita, Y.

(1933) Studies on a freshwater foettingeriid Hyalospira caridinae. Japan J. Zool., 4:439.

:

ciliate,

Chapter 38

Order 2 Spirotricha Blitschli

With
free cilia only; exceptionally with small groups of cirrus-like pro-

jections in addition to cilia

Uniformly ciliated; in Peritromidae dorsal surface without or with a few cilia; in Licnophoridae cilia only on edge of attaching disk; peristome usually extended; peristomal field mostly ciliated Suborder 1 Heterotricha Ciliation much reduced or none at all

Rounded

in cross-section; cilia usually much reduced; adoral zone encloses a non-ciliated peristomal field in spiral form Suborder 2 Oligotricha (p. 814)

Compressed; carapaced; peristomal zone reduced to 8 membranellae which lie in an oval hollow. .Suborder 3 Ctenostomata (p. 829) Cirri only, on ventral side; dorsal side usually with rows of short bristles. Suborder 4 Hypotricha (p. 832)
.

Suborder

Heterotricha Stein

Body

complete and uniformly the same Peristome sunk in a funnel-like hollow at anterior end, thus mostly Family 1 Bursariidae (p. 797) covered Peristome lies almost completely free, leading to a short and narrow oral funnel (absent in one family) Peristome in anterior region A narrow non-ciliated zone on right of adoral zone; usually an undulating membrane or ciliary row to right of this non-ciliated zone and anterior to cytostome; a small peristomal field between the membrane and adoral zone Adoral zone extends diagonally to posterior-right on ventral surface; highly developed forms, with a long zone twisting Family 2 Metopidae (p. 800) spirally around body Adoral zone parallel to body axis on flat ventral surface, turns somewhat to right in front of cytostome; oral funnel distinct; typically an undulating membrane or a double ciliated furrow in front of cytostome Family 3 Spirostomidae (p. 801) Without the non-ciliated zone; a large peristomal field with a half or completely spiral adoral zone Peristomal field not ciliated; with a large undulating membrane Family 4 Condylostomidae (p. 806) on its right edge Peristomal field ciliated; without undulating membrane Peristomal field not drawn out in 2 wings; free-swimming or
ciliation

secretes gelatinous lorica

Family 5 Stentoridae (p. Peristomal field drawn out into 2 wings; with flask-shaped, pseudochitinuous lorica .. Family 6 Folliculinidae (p. Peristome at posterior end; cytopharynx directed anteriorly Family 7 Clevelandellidae (p.
796

806) thin

807)
809)

SPIROTRICHA, HETEROTRICHA
Body
ciliation either confined to ventral side or lacking

797

Free-living; flattened; cilia only on ventral surface; adoral zone surrounds anterior region of ventral surface; cytostome on left edge Family 8 Peritromidae (p. 810) near the middle of body Ectocommensal; extremities discoid; body narrowed; anterior disk

surrounded spirally by adoral zone; posterior disk bears memFamily 9 Licnophoridae (p. 810) branous cilia

Family

Bursariidae Perty

Genus

Bursaria Miiller.

Ovoid; anterior end truncate, posterior

end broadly rounded; dorsal surface convex, ventral surface flattened; deep peristome begins at anterior end and reaches about

Fig. 340.
tion,

a,

Bursaria truncatella,
;

X60
e,

X440 (Schewiakoff ) Balantidium duodeni, X170

c,

Bursaridium

(Stein);

(Kahl); b, Thylacidium truncadifficile, X210 (Kahl); d, B. praenucleatum, X950 (Kudo

and Meglitsch).
it gives rise to cytostome and cytopharynx, which is bent to left lengthwise fold divides peristome into 2 chambers; striation longitudinal; ciliation complete and uniform; macronucleus band-form; many micronuclei; many contractile vacuoles distributed along lateral and posterior borders; cysts with a double envelope; fresh water. Cytology and conjugation (Poljansky, 1934); division (Schmahl, 1926); fibrils (Peschkowsky, 1927).

central part of body, where

79S

PROTOZOOLOGY

B. truncatella M. (Fig. 340, a). 500-1000 m long; macronucleus a long rod; 10-34 vesicular micronuclei; fission mostly during night;
feeds on various Protozoa; cysts 120-200^ in diameter; macronucleus

becomes

coiled

and intertwined; fresh water (Schmahl, 1926;

to Bursaria in general

Beers, 1948).

Genus Thylacidium Schewiakoff. Similar

appearance; but smaller in size; peristome simple in structure without longitudinal fold; with zoochlorellae; fresh water. One species.
T. truncatum S. (Fig. 340,
b).

60-100/x long.
to Bursaria; peristome

Genus Bursaridium Lauterborn. Similar

funnel turns to right fresh water.
;

B.

difficile

Kahl

(Fig. 340, c). Anterior

end truncate, cyto pharynx

slanting toward right; about 130ju long.

Fig. 341. Balantidium coli, X530 (Kudo), a, a living trophozoite; b, a stained trophozoite; c, a fresh cyst; d, a stained cyst.

Genus Balantidium Claparede and Lachmann (Balantidiopsis

Butschli; Balantiodoides Alexeieff). Oval, ellipsoid to subcylindrical;

peristome begins at or near anterior end; cytopharynx not well developed; longitudinal ciliation uniform; macronucleus elongated; a

micro nucleus; contractile vacuole and cytopyge terminal; in the gut of vertebrates and invertebrates. Numerous species (Hegner, 1934;

Kudo and
B.
coli

Meglitsch, 1938).

(Malmsten)

(Fig. 341).

Ovoid; 40-80/x by 30-60m, but

slightly obliquely

length varies 30-150/z;

longitudinal rows of

body covered by many

with coarser

cilia;

peristome small near anterior tip, lined inconspicuous cytostome and cytopharynx are
cilia;

located at the end of peristome; 2 contractile vacuoles, one terminal,

the other near the middle of body; macronucleus sausage-shape and a vesicular micro nucleus; cytopyge near the posterior tip; food
particles are of various kinds, including erythrocytes

and other host

SPIROTRICHA, HETEROTRICHA
cell

799

multiples

fragments, starch grains, faecal debris, etc. The trophozoite by binary fission. Conjugation (Brumpt, 1909; Jameson,
cysts are circular to ovoid in outline; slightly yellowish or

1927; Scott, 1927; Nelson, 1934).

The

greenish and refractile; 40-60ju in diameter; cyst wall

made up

of 2

membranes; cytoplasm hyaline; macronucleus and a

vacuole are usually seen.

contractile

This

ciliate lives in

the colon and caecum of

man and
made

causes
first

balantidiosis or balantidial dysentery. Strong (1904)

histological study of the infection.

the

and blood vessels of the there is hyperaemia with punctiform haemorrhages, and later vascular dilatation, round cell infiltration, eosinophilia, etc., develop in
the infected area. Finally deep-seated ulcers are produced.
antidial dysentery
is

The organisms invade the tissues mucosa and submucosa. At the beginning

The

bal-

usually of chronic type. It has a wide geograph-

ical distribution. In the United States a few cases of infections have been observed in recent years. In the Philippine Islands, more cases have been noticed than anywhere else. This ciliate is a very common parasite in the intestine of pigs, and also of chimpanzee and orang-outang. In pigs, the organism ordinarily confines itself to the lumen of the intestine, but according to Ratcliffe (1934), when the host animals become infected by organisms belonging to Salmonella, it invades and ulcerates the intestinal wall. The cysts developing in pigs appear to become the chief source of infection, since balantidial dysentery is more commonly found among those who come in contact with pigs or pig intestine. The cysts remain viable for weeks in pig faeces in moist and dark places, though they are easily killed by desiccation or exposure to sun light. The cysts may reach human mouth in food or in water contaminated with them, through unclean hands of persons

who come

in contact with faeces or intestine of pigs,

and

in

some

cases perhaps through

uncooked sausage.

B. suis McDonald. Ellipsoid; 35-120/z by 20-60/x; macronucleus more elongate than that of B. coli; in the intestine of pigs (McDonald,

1922). Levine (1940) through a series of culture studies, has to consider that B. coli

come

and B.

suis are only morphological

is

variations due to the nutritional condition and that B. suis

sy-

nonymous with B.
in cultures started

coli.

Lamy and Roux (1950)

observed both forms

with single individuals, and considered the elon-

gate suis as conjugants and the oval coli as vegetative forms.

B. caviae Neiva, da
guinea-pig.

Cunha and

Travassos. In the caecum of

Morphology

(Scott, 1927; Nie, 1950).

800

PROTOZOOLOGY

Other domestic and wild animals harbor various species of Balantidium.

B. duodeni Stein (Fig. 340, d). 70-80/x by 55-60^; in the intestine of
the frog.

B. praenucleatum

Kudo and

Meglitsch (Fig. 340,

e).

42-127ju long,

32-102/x thick, 25-80ju wide; macronucleus close to anterior end; in

the colon of Blatta orientalis (Kudo and Meglitsch, 1938).

Family 2 Metopidae Kahl

Genus Metopus Claparede and Lachmann. Body form changeable; when extended oblong or fusiform; peristome conspicuous, slightly spirally diagonal, beginning at the anterior end and reaching the
middle of body; when contracted, peristome much spirally coiled; cytopharynx short; body ciliation uniform, longitudinal or in some, spiral; longer cilia at ends; conspicuous contractile vacuole terminal; macronucleus ovoid to elongate; fresh or salt water (sapropelic),

some

parasitic.
es

Numerous

species.

Muller (M. sigmoides C. and L.) (Figs. 87; 342, a). 120-200^ long; sapropelic. Noland's (1927) study on its conjugation has been
described
(p. 161).

M.

M. M.
;

striatus

McMurrich

(Fig. 342, b). 80-120/x long; fresh water.

c).

fuscus Kahl (Fig. 342,

180-300m long by

60/x

wide and

40ju

thick fresh water.

M.

circumlabens Biggar (Fig. 342,

digestive tract of sea urchins,

d). 70-165ju by 50-75/x; in the Diadema setosum and Echinometris

subangularis in

Bermuda

(Biggar, 1932; Lucas, 1934); in Centrechi-

nus antillarum, etc., in Tortugas (Powers, 1935); in Diadema setosum and Echinometra oblonga in Japan (Uyemura, 1933). Genus Spirorhynchus da Cunha. Fusiform; somewhat flattened; anterior end drawn out and curved toward left; posterior end also drawn out; spiral peristome; cytopharynx small with an undulating

membrane;

cilia

tudinally striated;

uniformly long; contractile vacuole posterior; longibody surface with closely adhering bacteria

(Kirby); three spherical macronuclei; micronucleus (?); in brackish water (da Cunha, 1915). S. verrucosus da C. (Fig. 342, e). 122-140^ by 20-22^. Kirby (1934) observed it in salt marsh with 3 per cent salinity; California. Genus Caenomorpha Perty (Gyrocoris Stein). Bell-shaped; carapaced ectoplasm in some species bears protricho cysts; strong marginal zone of about 8 rows of cilia; 1-2 dorsal rows of longer cilia and a dense spiral field around caudal prolongation; peristome long; cytostome posterior; cytopharynx directed anteriorly; a single

SPIROTRICHA, HETEROTRICHA
d

801

Fig. 342. a,
c,

Metopus

es,

X260 (Kahl);

b,

M.

striatus,

X220 (Kahl);

M.fuscus, X150 (Kahl); d, M. circumlabens, X370 (Powers^; e, Spirorhynchus verrucosus, X360 (Kirby); f, Caenomorpha medusula, X200 (Blochmann); g, Blepharisma lateritium, X160 (Penard); h, B. persicinum, X290 (Penard); i, B. steini, X340 (Penard); j, Protocruzia pigerrima, X390 (Faria, da Cunha and Pinto); k, Phacodinium metschnicofli,

X270

(Kahl).

elongate or two spherical macro nuclei; a micro nucleus; fresh or salt

water (sapropelic). Several species. C. medusula P. (Fig. 342, /). 150/x by

water. Several varieties.

130/x; fresh

and brackish

Family 3 Spirostomidae Kent.

Genus Spirostomum Ehrenberg. Elongated; cylindrical; somewhat compressed; ectoplasm with highly developed myonemes which
are arranged lengthwise independent of ciliary rows, hence highly
contractile; yellowish to

brown; excretory vacuole terminal

large,

with a long dorsal canal; macro nucleus either ovoid or chain form;

802
cilia

PROTOZOOLOGY
short; rows longitudinal; caudal cilia are thigmotactic, secrete
;

mucous threads (Jennings) peristome

closely lined with short

mem-

branellae; fresh or salt water. Several species.

Fig. 343. a, Spirostomum ambiguum, X65 (Kahl); b, S. minus, X140 (Kahl); c, S. loxodes, X240 (Stokes); d, S. intermedium, X140 (Kahl); e, S. teres, X200 (Kahl); f, S. filum, X190 (Penard); g, Gruberia calkinsi, X140 (Bertran); h, Pseudoblepharisma tenuis, X310 (Kahl); i, Parablepharisma pellitum, X 340 (Kahl).

SPIROTRICHA, HETEROTRICHA
S.

803

ambiguum E.

(Figs. 38; 343, a). 1-3

mm.

long; macronucleus

composed of many beads; many micronuclei; peristome 2/3 the body length; fresh water. Regeneration (Seyd, 1936); irritability
(Blattner, 1926).
S.

minus Roux

(Fig.

343,

b).

500-800/x

long;

macronucleus
(length: width,

chain-form; in fresh and salt water (Kahl).

S. loxodes Stokes (Fig. 343, c).

About 300m long

6-7:1); peristome about 1/3 the body length; oblique striation;

longer
S.
cilia at ends; macronucleus chain-form; fresh water. intermedium Kahl (Fig. 343, d). Slender; 400-600/x long; macronucleus chain-form; fresh water.

S. teres Claparede and Lachmann (Fig. 343, e). 150-400m long; macronucleus oval; in fresh water and also reported from salt water. S. filum (E.) (Fig. 343, /). Peristome 1/4 the body length; posterior end drawn out; 200-300/* up to 700/t long; fresh water. Genus Gruberia Kahl. Similar to Spirostomum in general appearance; but posterior end drawn out; slightly contractile; contractile vacuole posterior; macronucleus compact or beaded salt water. G. calkinsi Beltran (Fig. 343, g). 200-800^ long; peristome 2/3
;

the

body length; many

(contractile?) vacuoles distributed; monili-

form macronucleus; many micronuclei; Woods Hole (Beltran, 1933). Genus Blepharisma Perty. Pyriform, spindle-form or ellipsoid; somewhat narrowed anteriorly; compressed; peristome on the left border, which is twisted to right at posterior end and connected with oral funnel with membrane; in front of cytostome a 2-layered undulating membrane on right edge; ciliary rows longitudinal; ciliation dense; contractile vacuole and cytopyge terminal; macronucleus one or divided into several parts; several species rose-colofea
1

fresh or salt water.

Many species.

B. lateritium (Ehrenberg) (Fig. 342, g). 130-200/z long; pyriform; macronucleus oval; a micro nucleus; rose-colored; fresh water among decaying leaves. B. persicinum P. (Fig. 342, A). 80-1 20ju long; elongate oval;
posterior end pointed; left peristomal edge sigmoid; preoral membrane large; macronucleus in 3-7 parts; rose-colored; fresh water among decaying vegetation. B. steini Kahl (Fig. 342, i). 80-200^ long; macronucleus ovoid; reddish to colorless; fresh water in sphagnum. B. undulans Stein. 150-300/z long; macronucleus in 2 parts; undulating membrane long; cytopharynx directed posteriorly; fresh water among decaying vegetation. Contractile vacuole (Moore,

1934); influence of light on color (Giese, 1938)

(p.

46);

morphology

804

PROTOZOOLOGY
(Stolte, 1924)
;

and physiology

macronuclear reorganization (Young,

1939); multiconj ligation (Weisz, 1950a); zoopurpurin (Weisz, 1950). Genus Protocruzia Faria, da Cunha and Pinto. Peristome does

not turn right, leads directly into cytostome; convex left side not ciliated, but bears bristles; flat right side with 3-5 faintly marked ciliary rows; peristome begins at pointed anterior end and extends

1/4-1/3 the body length; cyto pharynx

(?);

macro nucleus simple;

contractile vacuole subterminal; salt water.

P. pigerrima (Cohn) (Fig. 342, j). About 20m (da Cunha); 5060^ long (Kahl) peristome 1/4-1/3 the body length; salt water. Genus Phacodinium Prowazek. Oval; marked grooves on body surface; cilia in cirrus-like fused groups; peristome long on left margin; cytostome posterior; contractile vacuole terminal; macronucleus horseshoe-shape; 5-9 micronuclei; fresh water. One species.
;

P. mctschnicoffi, (Certes) (Fig. 342, k). About 100m long. Genus Pseudoblepharisma Kahl. Body form intermediate between Spirostomum and Blepharisma; right peristomal edge with 2

rows of cilia; fresh water. P. tenuis K. (Fig. 343, h). 100-200m long. Genus Parablepharisma Kahl. Similar to Blepharisma; but peristome-bearing anterior half narrowed neck-like and pointed; ectoplasm covered with gelatinous layer in which symbiotic bacteria are

imbedded

salt water.
i).

P. pellitum K. (Fig. 343,

120-180m long.

Genus Nyctotherus Leidy. Oval or reniform; compressed; peristome begins at anterior end, turns slightly to right and ends in cytostome located midway between the ends; cyto pharynx runs dorsally and posteriorly, a long tube with undulating membrane; ciliary rows longitudinal and close-set; massive macronucleus in
anterior half with a micronucleus
;

in

some, nuclei are suspended

by a karyophore; endoplasm with

in anterior region,

discoid glycogen bodies, especially

hence yellowish to brown; contractile vacuole

in the colon of

and cytopyge terminal;

invertebrates.

Numerous

species

Amphibia and various (Geiman and Wichterman, 1937;

Wichterman, 1938; Carini, 1938-1945). N. ovalis L. (Figs. 3; 344, a, b). Ovoid; anterior half compressed; macronucleus elongate, at right angles to dorso-ventral axis at
anterior 1/3; micronucleus in front of macronucleus; distinct karyophore; glycogen bodies; 90-185m by 62-95m; giant forms up to 360m

by 240m; cysts 72-106m by 58-80m;

in the colon of cockroaches.

The

chromatin spherules of the macronucleus are often very large Fibrillar structure (ten Kate, 1927); nuclei (Kudo, 1936).

(p. 42).

SPIROTRICHA, HETEROTRICHA

805

N. cordiformis (Ehrenberg) (Figs. 85; 344, c). 60-200m by 40-140^; ovoid; micronucleus behind macronucleus; no karyophore; in the colon of frogs and toads. Higgins (1929) notes that there are certain differences between American and European forms and that the

Nydotherus ovalis, X340 (Kudo); c, N. cordiformis Condylostoma vorticella, X 120 (Penard) e, Stentor coerul(Roux); eus, somewhat contracted, X70 (Roux); f, S. polymorphus, X60 (Roux); i, S. igneus, X160 g, S. mulleri, X50 (Kahl); h, S. roeseli, X75
Fig. 344.
a,
;

b,

X 170

(Stein)

d,

(Kahl);

j,

S. amethystinus,

X100

(Kahl).

806

PROTOZOOLOGY

organisms exhibit a great variety of form and size in the tadpoles of various frogs, although those of adult frogs are relatively constant in form. Life cycle (Wichterman, 1936) (p. 198) tactile cilia (Fernandez-Galiano, 1948); fibrillar structure (ten Kate, 1927).
;

Family 4 Condylostomidae Kahl

Genus Condylo stoma Bory.

Ellipsoid;

anterior end truncate,

posterior end rounded or bluntly pointed; slightly flattened; peri-

stome wide at anterior end and V-shaped, peristomal field not ciliated; a large membrane on right edge and adoral zone on left; macronucleus moniliform; one to several contractile vacuoles often with canal; cytopyge posterior; fresh or salt water. Many species (Spiegel,

1926).

C. vorticella (Ehrenberg) (Fig. 344, d). 100-200/x long; fresh water. C. patens (Mtiller). 250-550ju long; salt water;
kins).

Woods Hole

(Cal-

Family 5 Stentoridae Carus

Genus Stentor Oken. When extended, trumpet-shaped or cylindrical; highly contractile; some with mucilaginous lorica; usually oval to pyriform while swimming; conspicuous peristomal field frontal;
adoral zone encircles peristome in a spiral form, leaving a narrow

gap on ventral side; the zone and field sink toward cytostome and the former continues into cytopharynx; macro nucleus round, oval or elongated, in a single mass or moniliform; contractile vacuole anterior-left; free-swimming or attached; fresh water. S. coeruleus Ehrenberg (Figs. 14; 344, e). Fully extended body 1-2 mm. long; anterior end greatly expanded; the beautiful blue color is due to a pigment, stentorin, lodged in interstriation granules (p. 45); macronucleus moniliform; fresh water. Body and nuclear size (Burnside, 1929); physiology (Dierks, 1926); effect of en-

vironment

(Stolte, 1922); cytology (Dierks, 1926; Weisz, 1949); regeneration (Schwartz, 1935; Weisz, 1948, 1948a, 1951); vertical dis-

tribution (Sprugel, 1951).

S. striatus Barraud-Maskell.

Dark

bluish green; funnel-shaped;

peristomal edge irregularly undulating; striation conspicuous; macro-

nucleus beaded; up to 2.2

S.

mm.

long.

polymorphic (Muller)

(Fig. 344, /). Colorless;

with symbiotic

Chlorella 1-2
terior

mm.

long

when extended; macronucleus beaded; an-

end expanded.

S. miilleri (Bory) (Fig. 344, g). Colorless; with zoochlorellae; 2-3

mm.

long; anterior end expanded; posterior portion

drawn out

into

SPIROTRICHA, HETEROTRICHA
stalk, often

807

housed in a gelatinous tube; on body surface 3-4 longer grouped among cilia; macronucleus moniliform. S. roeseli Ehrenberg (Fig. 344, h). 0.5-1 mm. long; anterior end expanded; body surface with groups of longer cilia; posterior portion drawn out and often housed in a gelatinous tube; macronucleus long band-form.

and

stiff cilia

S. igneus E. (Fig. 344,

i).

Rose-colored or colorless; 200-4CHV

long; macronucleus oval; ciliation uniform.

S. niger (Miiller). Yellowish or

brown; macronucleus oval; 200-

300/x long.

S. multiformis (M.) Dark blue to bluish green; anterior end not expanded; 150-200^ long; macronucleus oval. S. amethystinus Leidy (Fig. 344, j). Habitually pyriform (contracted); amethyst-blue; with zoochlorellae; 300-600/z long; macro-

nucleus oval.
S. pyriformis

Johnson.

When

extended 500/x long; anterior end

200/x in diameter.

Genus Fabrea Henneguy. Pyriform; posterior end broadly roundanterior end bluntly pointed; peristome extends down from anterior end 2/5 or more the body length, its posterior portion closely wound; peculiar black spot beneath membranellae in anterior portion of spiral adoral zone, composed of numerous pigment graned,
ules;

without contractile vacuole; macronucleus, a sausage-shaped

in 4 parts; in salt water.

body or
450/z

F. salina

H.

(Fig. 345, a, b). 120-220/*

by

67-125/i (Kirby); 130-

by

70-200/x (Henneguy); cysts ovoidal, with gelatinous enve-

lope; 89-1 11m

by

72-105ju.

Kirby (1934) found the organism

in

ditches and pools in salt marshes, showing salinities 7.5-20.1 per

cent in California.

Genus Climacostomum Stein. Oval; flattened; right edge of peristome without membrane, left edge, semicircular or spiral with a strong adoral zone; peristomal field ciliated; cytopharynx a long curved tube with a longitudinal row of cilia; macronucleus bandform; contractile vacuole terminal, with two long canals; fresh or
brackish water.
C. virens (Ehrenberg) (Fig. 345,
c).

100-300/x long; with or without

zoochlorellae; fresh

and brackish water.

Family 6 Folliculinidae Dons

Genus
d)

Folliculina

Lamarck. Horny or chitinous

lorica (Fig. 345,

attached on broad surface; neck of the lorica oblique to perpendicular; sometimes with a collar or spiral ridge; neck uniform in

808

PROTOZOOLOGY

Fig. 345.

a, b,

Fabrea salina (Kirby)

(a,

trophozoite,

XI 70;
X50

b, cyst,

X330);
of
f,

Climacostomum vireus, X100 (Stein); d, side-view of the lorica a Folliculina, X150 (Andrews); e, Folliculina moebiusi, X170 (Stein);
c,

F. producta,

XI 10

(Wright);

g,

Pseudofolliculina arctica,

(Dons);

h, Parafolliculina violacea,

X230 (Andrews).

diameter; in salt or fresh water. Species (Andrews, 1914, 1921, 1923;

Sahrhage, 1916); test secretion (Dewey, 1939). F. moebiusi Kahl (Fig. 345, e). Lorica about 500^ long. F. producta (Wright) (Fig. 345,/). Lorica yellowish brown; 250/x
long; neck often long; Atlantic coast. F. boltoni Kent. Lorica about 200/z; lorica and body blue green; aperture only slightly enlarged; short neck oblique or upright; in
fresh water (Hamilton, 1950, 1952).

Genus Microfolliculina Dons. Posterior end or

sack-like protuberances.

sides of lorica with

M.

limnoriae (Giard).

Lorica dark blue; pellicle faintly striated;

its

salt water.

Genus Pseudofolliculina Dons. Lorica attached with

posterior

SPIROTRICHA, HETEROTRICHA

809

end; more or less vertical; without ring-furrow in middle; with or without style; salt water.
ridge; off

P. arctica D. (Fig. 345, g). Lorica about 43(V high, with spiral Norweigian coast 15-28 m. deep.

Genus Parafolliculina Dons. Neck of lorica with a basal swelling; attached either with posterior end or on a lateral surface; salt water.
P. violacea (Giard) (Fig. 345,
h).

Total length 225-288 /x; widely

distributed in salt water (Andrews, 1921, 1942).

Family 7 Clevelandellidae Kidder

Genus Clevelandella Kidder

(Clcvelandia K.) Elongate pyriform

.

or spear-shaped; posterior region

drawn out, at the end of which peristome and cytostome are located; body more or less flexible; completely ciliated; one macro nucleus supported by a karyophore;
a micro nucleus; a contractile vacuole at posterior
left,

near cytopyge;

*m0
a, b, ventral and dorsal views of Clevelandella panesthiae, Paraclevelandia brevis (c, ventral view, X760; d, a cyst, X740) (Kidder); e, Peritromus californicus, X360 (Kirby); f, Lichnophora macfarlandi, X420; g, L. conklini, X340 (Stevens).

Fig. 346.
c, d,

X300;

810

PROTOZOOLOGY
in the colon of

endocommensals

wood-feeding roaches, Panesthia

javanica and P. spadica. Several species.

C. panesthiaeK. (Fig. 346, a, b). Broadly fusiform with bluntly

pointed anterior end and truncate posterior end;

by

53-78(62)ju; peristomal
is

projection

87-156 (123)^ about one-fifth the body

length; peristome

nearly enclosed; macro nucleus massive; a vesi-

its anterior border; karyophore separates the endoplasm into 2 parts: anterior part with glycogenous platelets, posterior part with numerous food particles; often parasitized by Sphaerita (p. 893); in the colon of Panesthia javanica and P. spadica

cular micro nucleus

on

(Kidder, 1937, 1938).

Genus Paraclevelandia Kidder. Elongate pyriform; body

rigid;

posterior end truncated obliquely to left; no peristomal projection;

one macro nucleus and one micro nucleus; at anterior end, there is a sac connected with the karyophore, which is said to be a "macronuclear reservoir"; endocommensals. P. brevis K. (Fig. 346, c-d). Conical in shape; 16-38 (38)/z by 9-21 (19)m; macronucleus spherical to elongate ellipsoid; micro nucleus comparatively large, retains nuclear stains longer than macronucleus; anterior sac may sometimes be absent; cysts, 14-19/z long; ovoid; with a spherical macronucleus and a micro nucleus; in the colon of Panesthia javanica and P. spadica (Kidder, 1938).

Family 8 Peritromidae Stein

Genus Peritromus
surface with
ciliary

Stein. Ovoid; ventral surface flattened, dorsal

hump

of irregular outline bearing a few

stiff cilia;

rows only on ventral surface; a small undulating membrane at posterior end of peristome; short marginal spines; 2 macro- and 2
micro-nuclei; salt water.

90-10CV long; creeping on bottom; Woods Hole. e). Peristome short; left margin slightly concave; dorsal hump with wart-like protuberances, bearing spines (about 12/z long); 16-19 or more ventral ciliary rows; 2 spherical macronuclei, one anterior right and the other posterior left of hump; micronuclei 4 (2-5); 89-165^ by 60-96/i; salt marsh pools with salinity "1.2-6 per cent" in California (Kirby, 1934).
P.

emmae

S.

P. californicus Kirby (Fig. 346,

Family 9 Licnophoridae Stevens

into basal disc, neck

Genus Licnophora Claparede. Discoid; body roughly divisible and oral disc; basal disc for attachment, with

several concentric ciliary coronas; neck flattened, contractile nar-

rowed part with or without a ventral furrow and fibril-bundles (both running from oral groove to basal disc) oral disc highly flat;

SPIROTRICHA, HETEROTRICHA

811

tened, round or ovoid; edge with membranelle zone which extends

to
tractile vacuole;

pharyngeal funnel; macro nucleus long chain-form; without concommensal in salt water animals. L. macfarlandi Stevens (Fig. 346, /). Average 90-1 10m by 45-60/t;
;

diameter of basal disc 40-45/1 basal disc circular; macronuclei in 25-35 parts in 4 groups; commensal in the respiratory tree of Sticho-

pus

californicus (Stevens, 1901).

Morphology,

fission

and regenerain Crepidula

tion (Balmuth, 1941, 1942).

L. conklini S. (Fig. 346, g). 100-135/* long;

commensal

plana of Atlantic coast.

References

Andrews,

E. A.: (1914) The bottle-animalcule, Folliculina; ecological notes. Biol. Bull, 26:262. (1921) American Follinulinas: taxonomic notes. Am. Nat., 55:347. (1923) Folliculina: case making, anatomy and transformation. J. Morphol., 38:207. (1942) Parafolliculina violacea at Woods Hole. Biol. Bull., 83:91. Balamuth, W. (1941) Studies on the organization of ciliate Protozoa. I. J. Morphol., 68:241. (1942) II. J. Exp. Zool., 91 15. Beers, C. D.: (1948) Encystment in the ciliate Bursaria truncatella. Biol. BuR., 94:86. Beltran, E.: (1933) Gruberia calkinsi, etc. Ibid., 64:21. Biggar, Ruth B.: (1922) Studies on ciliates from Bermuda sea urchins. J. Parasitol., 18:252. Blattner, H.: (1926) Beitrage zur Reizphysiologie von Spirostomum ambiguum. Arch. Protist., 53:253. Brumpt, E. (1909) Demonstration du role pathogene du Balantidium coli et conjugaison de cet infusoire. C. R. Soc. biol., 67: 103. Carini, A. (1938) Sobre um Nyctotherus da intestino de um grillotalpideo. Arch. Biol., 22, 1 p. (1938a) Sobre um Nyctotherus da intestino da "Testudo tabulata." Ibid., 22, 2 pp. (1939) Sobre um Nyctotherus da cloaca de uma Amphisbaena. Ibid., 23, 1 p. (1940) Contribuicao ao estudo dos nictoteros dos batraquios do Brasil. Ibid., 24, 15 pp. (1945) Sobre um Nyctotherus do Crossodactylus gaudichaudi. Ibid., 29, 2 pp. da Cunha, A. M.: (1915) Spirorhynchus verrucosus, etc. Brazil Medico, 19:3. Dewey, Virginia C: (1939) Test secretion in two species of Folliculina. Biol. Bull., 77:448. Dierks, K.: (1926) Untersuchungen uber die Morphologie und Physiologie des Stentor coeruleus, etc. Arch. Protist., 54: 1. Fernandez-Galiano, D.: (1948) Los cilios tactiles de Nyctotherus
:

812

PROTOZOOLOGY
cordiformis. Bol. Real Soc. Espan. Hist. Nat., 46:219.
:

Geiman, Q. M. and Wichterman, R. (1937) Intestinal Protozoa from Galapagos tortoises. J. Morphol., 23:331. Hamilton, J. M.: (1950) A f olliculinid from northwestern Iowa. Science, 111:288. (1952) Studies on loricate Ciliophora.

Proc.

Iowa Acad. Sc,

58:469. Hegner, R.

(1934) Specificity in the genus Balantidium based etc. Am. J. Hyg., 19:38. (1940) Nyctotherus beltrani, etc. J. Parasitol., 26:315. Higgins, Helen T.: (1929) Variation in the Nyctotherus found in frog and toad tadpoles and adults. Tr. Am. Micr. Soc, 48: 141.
:

W.

on

size

and shape,

Jameson, A.

P.: (1927) The behavior of Balantidium coli in cultures. Parasitology, 19:411. Kahl, A.: (1932) Urtiere oder Protozoa. Dahl's Die Tierwelt

Deutschlands,

etc.

Part

15.

Kidder, G. W.: (1937) The

Protozoa of the wood-feeding roach Panesthia. Parasitology, 29:163. (1938) Nuclear reorganization without cell division in Paraclevelandia simplex, etc. Arch. Protist., 91:69. Kirby, H. Jr.: (1934) Some ciliates from salt marshes in California. Ibid., 82:114. Kudo, R. R.: (1936) Studies on Nyctotherus ovalis, with special reference to its nuclear structure. Ibid., 87: 10. and Meglitsch, P. A.: (1938) On Balantidium praenucleatum, etc. Ibid., 91:111. Lamy, L. and Roux, H.: (1950) Remarques morphologiques, biologiques et specifiques sur les Balantidium de culture. Bull. Soc. Path. Exot., 43:422. Levine, N. D. (1940) The effect of food intake upon the dimensions of Balantidium from swine in culture. Am. J. Hyg., 32:81.
intestinal
:

Lucas, Miriam S.: (1934) Ciliates from Bermuda sea urchins. I. J. Roy. Micr. Soc, 54:79. McDonald, J. D. (1922) On Balantidium coli and B. suis (sp. nov.). Univ. California Publ. Zool., 20:243. Moore, Imogene: (1934) Morphology of the contractile vacuole and cloacal region of Blepharisma undulans. J. Exper. Zool., 69:59. Neiva, A., da Cunha, A. M. and Travassos, L.: (1914) Parasitologische Beitrage. Mem. Inst. Oswaldo Cruz, 6:180. Nelson, E. C. (1934) Observations and experiments on conjugation of the Balantidium from the chimpanzee. Am. J. Hyg., 20: 106. Nie, D.: (1950) Morphology and taxonomy of the intestinal Protozoa of the guinea-pig, Cavia porcella. J. Morphol., 86:381. Noland, L. E. (1927) Conjugation in the ciliate, Metopus sigmoides. J. Morphol. Physiol., 44:341. Peschkowsky, Ludmilla: (1927) Skelettgebilde bei Infusorien.
:
:

Arch. Protist., 56:31.

Poljansky, G.: (1934) Geschlechtsprozesse bei Bursaria

Ibid., 81:420.

truncatella.

Powers,

P. B. A.: (1936) Studies on the Papers Tortugas Lab., 29:293.

ciliates of sea urchins, etc.

Sahrhage, H.: (1916) Ueber

die Organisation

und

die Teilungsvor-

SPIROTRICHA, HETEROTRICHA
tist.,

813

gang des Flaschentierchens (Folliculina ampulla). Arch. Pro37:139.

0.: (1926) Die
bei Teilung von 54 359. Schwartz, V.: (1935) Versuche uber Regeneration und Kerndi-

Schmahl,

Neubildung des Peristoms

Ibid.,
:

Bursaria truncatella.

morphismus bei Stentor coeruleus. Ibid., 85: 100. Scott, Miriam J.: (1927) Studies on the Balantidium from the guinea-pig. J. Morphol. Physiol., 44:417. Seyd, E. L.: (1936) Studies on the regulation of Spirostomum ambiguum. Arch. Protist., 86:454. Spiegel, A.: (1926) Einige neue marine Ciliaten. Arch. Protist., 55:
184.

Sprugel, G. Jr.: (1951) Vertical distribution

etc.

of Stentor coeruleus,

Ecology, 32:147. Stevens, N. M.: (1901) Studies on ciliate Infusoria. Proc. California Acad. Sc. Ser. 3, 3:1. (1903) Further studies on the ciliate Infusoria, Licnophora and Boveria. Arch. Protist., 3:1. Stolte, H.-A.: (1922) Der Einfluss der Umwelt auf Macronucleus und Plasma von Stentor coeruleus. Ibid., 45:344. (1924) Morphologische und physiologische Untersuchungen an Blepharisma undulans. Ibid., 48:245. Strong, R. P. (1904) The clinical and pathological significance of Balantidium coli. Bur. Gov. Lab. Manila., Biol. Lab. Bull.,
:

no. 26.

Tanabe, M. and Komada, K. (1932) On the cultivation of Balantidium coli. Keijo J. Med., 3:385. ten Kate, C. G. B.: (1927) Ueber das Fibrillensystem der Ciliaten.
:

Arch. Protist., 57:362.

Uyemura, M.:

(1933) On two ciliates: Entorhipidium tenue and Metopus circumlabens, etc. J. Nat. Hist. Soc. Tokio, 31: 5 pp. Weisz, P. B.: (1948) Time, polarity, size and nuclear content in the

regeneration of Stentor fragments. J. Exper. Zool., 107:269. (1948a) Regeneration in Stentor and the gradient theory. Ibid., 109:439. cytochemical and cytological study of differentia(1949) tion in normal and reorganizational stages of Stentor coeruleus. J. Morphol., 84:335. (1950) On the mitochondria nature of the pigmented granules in Stentor and Blepharisma. Ibid., 86: 177. - (1950a) Multiconjugation in Blepharisma. Biol. Bull., 98 242. (1951) An experimental analysis of morphogenesis in Stentor coeruleus. J. Exper. Zool., 116:231. Wichterman, R.: (1936) Division and conjugation in Nyctotherus cordiformis, etc. J. Morphol., 60:563. (1938) The present state of knowledge concerning the existence of species of Nyctotherus living in man. Amer. J. Trop. Med., 18:67. Woodruff, L. L.: (1935) Physiological significance of conjugation in Blepharisma undulans. J. Exper. Zool., 70:287. Young, Dixie: (1939) Macronuclear reorganization in Blepharisma undulans. J. Morphol., 64:297.

Chapter 39

Order 2 Spirotricha Biitschli (continued)

Suborder 2 Oligotricha Biitschli

number in the Oligotricha and the adoral zone encloses a non-ciliated spiral peristomal field.
cilia

HE

are greatly reduced in

Free-living

Oral portion of peristome

lies free

on ventral surface Family

field

Halteriidae
(p.

Adoral zone encloses frontal peristomal

Without lorica With lorica or

Parasitic

test'.

Family 2 Strobilidiidae Family 3 Tintinnidae

815)

(p.

816)

Adoral and dorsal zones, both directed anteriorly and retractile; no other cilia Family 4 Ophryoscolecidae (p. 816) In addition to adoral and dorsal zones, groups of cirri in posterior half of body, directed posteriorly and nonretractile

Family 5 Cycloposthiidae

(p.

823)

Family

Halteriidae Claparede and

Lachmann

Genus Halteria Dujardin. Spherical or broadly fusiform; anterior

border bears conspicuous adoral zone; oral part of peristome with a small membrane on right edge and cirri on left; with an equatorial zone of small oblique grooves, each bearing 3 long cirri or bristles;

macro nucleus oval; a micronucleus; contractile vacuole

stome; fresh water. Several species (Szabo, 1935).

left of

cyto-

H. grandinella

(Miiller)

(Fig.

347, a).

About

7 bristle-bearing

grooves; 15 frontal and 7 adoral membranellae; 20-40/x long. Kahl

(1932) distinguishes 2 varieties: var. cirrifera (Fig. 347,
long, with
b),

25-50ju

huge

cirri

instead of fine

body

cirri;

and

var. chlorelligera

(Fig. 347, c), 40-50/x long,

with bristles and large zoochlorellae;

to spher-

fresh water.

Genus Strombidium Claparede and Lachmann. Ovoid

ical;

adoral zone very conspicuous (2-4 conspicuous sickle-form

membranellae and adoral membranellae extend down cytopharynx, the first section surrounding an apical process); no body bristles or cirri; trichocysts; macronucleus oval or band-form; a micronucleus; a contractile vacuole; salt or fresh water. Numerous
frontal
species.

S. calkinsi
salt water;

Faur6-Fremiet

(Fig. 347, d). 35-60/z long; brackish

and

Calkins (1902)

first

observed
814

it

at

Woods

Hole.

SPIROTRICHA, OLIGOTRICHA
Genus Tontonia Faure-Fremiet. With well-developed
lar;

815
apical col-

a long cytoplasmic (contractile) caudal process; salt water.

(Fig.

T. gracillima F.-F.

347,

e).

48-52/z long; caudal process

250-300ju long; macronucleus moniliform; with zoochlorellae.

X490 (Kahl); b, H. g. var. cirrifera, X260 (Kahl); d, Strombidium (Calkins); e, Tontonia gracillima, X540 (Faure-Fremiet); f, Strobilidium gyrans, X340 (Kahl); g, Tintinnidium fluviatile, X140 T. semiciliatwn, X140 (Sterki); j, Strombidinopsis gyrans, (Kent); h, X270 (Kent); k, Tintinnopsis cylindrata, X440 (Daday); 1, T. illinoisensis, X420 (Hempel); m, Codonella cratera, X540 (Faur6-Fremiet).
Fig. 347.
a,

Halteria grandinella,
c,

X370 (Kahl); calkinsi, X900

i,

H.

g.

var. chlorelligera,

Family 2 Strobilidiidae Kahl

Genus Strobilidium Schewiakoff. Pyriform or turnip-shaped; cytostome at anterior end; without cytopharynx; horseshoe-shaped

816

PROTOZOOLOGY
;

macronucleus anterior; a micronucleus a contractile vacuole; fresh

or salt water. Several species (Busch, 1921).
S. gyrans (Stokes) (Fig. 347, /). Lateral

border with rounded

ele-

vation near anterior end, posterior end truncate; 40-70/x long; in

standing fresh water.

Family 3 Tintinnidae Claparede and Lachmann

Conical or trumpet-like, attached inside a lorica of various forms,

composed of gelatinous or pseudochitinous substances; with longitudinal rows of cilia, and 2 (1-4) macro- and a micro-nuclei; mostly pelagic, a few inhabiting fresh or brackish water. Kofoid and Campbell (1929) distinguished more than 300 species and placed them in 12 families and 51 genera, of which 23 genera were created by them. A few genera and species are mentioned here. Taxonomy (Hofker, 1932); species (Campbell, 1942; Balech, 1942-1951; Rampi, 1950;
Silva, 1950); factors in evolution (Kofoid, 1930); lorica

formation

(Busch, 1925).

Genus Tintinnidium Stein. Elongated lorica, highly irregular in form; soft; aboral end closed or with a minute opening; wall viscous and freely agglomerates foreign bodies; salt or fresh water. T.fluviatile Stein (Fig. 347, g). Lorica 100-200juby 45ju; on vegetation in fresh water.
T. semiciliatum Sterki (Fig. 347, h,
fresh water.
i).

40-60/z long;

on plants

in

Genus Strombidinopsis Kent. Lorica often absent; ovate or pyriform; frontal border with numerous long cirrus-like cilia; body covered by fine cilia; contractile vacuole posterior; fresh water. S. gyrans K. (Fig. 347, j). 30-80/1 long; fresh water pond. Genus Tintinnopsis Stein. Lorica bowl-shaped; always with a
broad aperture; aboral end closed; wall thin and covered with foreign
bodies; salt or fresh water. Species (Balech, 1945).
T. cylindrata Kofoid

and Campbell

(Fig. 347, k). Lorica 40-50/c

long; in lakes.
T. illinoisensis Hempel (Fig. 347, 1). Lorica 59/x long; in rivers. Genus Codonella Haeckel. Lorica urn- to pot-shaped; sharply divided externally and internally into a collar and bowl; collar with-

out spiral structure; in fresh water. C. crater a (Leidy) (Fig. 347, m). Lorica 60-70/i by of varieties are often mentioned.

40/x;

number

Family 4 Ophryoscolecidae Stein

Elongate oval, asymmetrical; with 1 or 2 (adoral and dorsal) zones of membranellae; in digestive tract of mammals. Sharp (1914)

SPIROTRICHA, OLIGOTRICHA
employed "forma"
to distinguish forms in

817

Entodinium with comwhich scheme was extended to the whole family by Dogiel (1927). It is most probable that many species are varieties of a single species as judged by the work of Poljansky and Strelkow (1934); but since information is still incomplete, the present work ranks various formae with species, in agreement with Kofoid and MacLennan (1930). The relationship between these oligotrichs and host ruminants has not definitely been determined, but it appears to be commensalism rather than symbiosis (Becker, Schulz and Emmerson, 1930; Mowry and Becker, 1930). Morphology (Bretschneider, 1934, 1935); contractile vacuoles (MacLennan, 1933); conjugation (Dogiel, 1925); numbers in cattle stomach (Dogiel and Fedorowa, 1929); fauna in

mon

characteristics, differing in certain others,

African antelopes (Dogiel, 1932); in yaks (Dogiel, 1934); in Indian goat (Das-Gupta, 1935); in Indian ox (Kofoid and MacLennan,
1930, 1932, 1933); in gaur (Kofoid and Christenson, 1934); in sheep, wild sheep and goat (Ferber and Fedorowa, 1929; Bush and Kofoid,
1948).
Stein. Ovoid; with adoral and dorsal zones membranellae; dorsal zone some distance behind anterior end, encircling 3/4 the body circumference at middle, broken on right ventral side; 3 skeletal plates extend over the body length on rightventral side; 9-15 contractile vacuoles in 2 (anterior and posterior) circles; macro nucleus simple, elongate; in the stomach of cattle, sheep, goat and wild sheep (Ovis orientalis cycloceros) Several species (Kofoid and MacLennan, 1933); neuromotor system (Fernan-

Genus Ophryoscolex

of

dez, 1949).

Dogiel (1927) designated the following species as 3 formae of

0. caudatus Eberlein.
0. Ucoronatus Dogiel (Fig. 348, a). 120-1 70m

by
by

81-90/*;

primary

spine 38-58/* long; in sheep.

O. caudatus Eberlein (Fig. 348, b). 137-162/* 80-98/*; preanal

spines 47-60/* long; in sheep, goat, and cattle.

O. quadricoronatus Dogiel (Fig. 348,
c).

128-180/*

by

86-100/*;

preanal spines 48-63/* long; in sheep and Ovis orientalis cycloceros.

Genus Caloscolex Dogiel. Ovoid; anterior end truncate, posterior end rounded with or without processes; 2 zones of membranellae;
dorsal zone encircles the
in the

body completely;

3 skeletal plates variously

modified; 7 contractile vacuoles in a single circle; nucleus elongate;

Camelus dromcdarius. Several species. D. (Fig. 348, d). 130-160/x by 73-90/*. Genus Entodinium Stein. Without dorsal zone; adoral zone at truncate anterior end; without skeleton; contractile vacuole ante-

stomach

of

C. cuspidatus

SIS

PROTOZOOLOGY

Fig. 348. a, Ophryoscolex bircoronatus, X340 (Dogiel); b, 0. caudatus, (Dogiel); c, 0. quadricoronatus, X340 (Dogiel); d, Caloscolex cuspidatus, X310 (Dogiel); e, Entodinium caudatum, X500 (Becker and Talbott); f, E. bursa, X390 (Schuberg); g, A?nphacanthus ovum-rajae, X350 (Dogiel).

X310

rior;

macronucleus, cylindrical or sausage-form, dorsal; micronucleus

anterior to middle and on left-ventral side of macronucleus; in cattle

and sheep. Numerous species (Kofoid and MacLennan, 1930; MacLennan, 1935). E. caudatum S. (Fig. 348, e). 50-8 0/z long; in cattle and sheep. E. bursa S. (Fig. 348, /). 55-114/* by 37-78/* (Schuberg); 80/x by 60/t (Becker and Talbott) in the stomach of cattle. Genus Amphacanthus Dogiel. Similar to Entodinium; but spinous processes at both anterior and posterior ends in stomach of Camelus
; ;

dromedarius.

One

species.
g).

A. ovum-rajae D. (Fig. 348,

46-55/z

by

32-48/z.

SPIROTRICHA, OLIGOTRICHA

819

Genus Eodinium Kofoid and MacLennan. Dorsal zone on the same level as adoral zone; without skeleton; macronucleus a straight, rod-like body beneath dorsal surface; 2 contractile vacuoles; in cattle and sheep. Several species. E. lobatum K. and M. (Fig. 349, a). 44-60m by 29-37m; in Bos indicus (Kofoid and MacLennan, 1932). Genus Diplodinium Schuberg. Adoral and dorsal zones at the

Fig. 349.

a,

Eodinium lobatum, X540 (Kofoid and MacLennan);

b,

Diplodinium dentatum, X250 (Kofoid and MacLennan); c, Eremoplastron bovis, X550 (Kofoid and MacLennan); d, Eudiplodinium maggii, X500 (Dogiel); e, Diploplastron affine, X320 (Dogiel); f, Metadmium medium,

X320

(Dogiel).

820

PROTOZOOLOGY
level;

same
its

without skeletal plates; macro-nucleus beneath right

side,

anterior third bent ventrally at an angle of 30-90; 2 contractile

species (Kofoid and MacLennan, 1932). D. dentatum (Stein) (Fig. 349, b). 65-82/* by 40-50/*; in cattle

vacuoles; in cattle, antelope, Camelus dromedarius, reindeer, goat.

Numerous

(including Bos indicus).

Genus Eremoplastron Kofoid and MacLennan. Adoral and

dorsal

zones at anterior end; a single narrow skeletal plate beneath right surface; triangular or rod-like macronucleus, anterior end of which
is

often bent ventrally; 2 contractile vacuoles; in cattle, antelope,

sheep, reindeer.

Numerous

species (Kofoid
c).

E. bovis (Dogiel) (Fig. 349,

sheep.

52-100/x

and MacLennan, 1932). by 34-50/*; in cattle and

at anterior

Genus Eudiplodinium Dogiel. Adoral and dorsal zones

end; a single, narrow, skeletal plate beneath right surface; rod-like macronucleus with its anterior end enlarged to form a hook opening dorsally; pellicle and ectoplasm thick; 2 contractile vacuoles with

heavy membranes and prominent pores; and MacLennan, 1932).

E. maggii (Fiorentini) (Fig. 349,
tle,

in cattle. Species (Kofoid

d).

104-255/*

by 63-1 70m;

in cat-

sheep and reindeer. Genus Diploplastron Kofoid and MacLennan. Adoral and dorsal zones at anterior end; 2 skeletal plates beneath right surface; macro-

nucleus narrow; rod-like; 2 contractile vacuoles below dorsal surface, separated from macronucleus. One species (Kofoid and MacLennan,
1932).

in

D. affine (Dogiel and Fedorowa) (Fig. 349, the stomach of cattle, sheep, and goat.

e).

88-120/x

by

47-65/*;

Genus Metadinium Awerinzew and Mutafowa. Adoral and dorzones at anterior end; 2 skeletal plates beneath right surface sometimes fused posteriorly; macronucleus with 2-3 dorsal lobes; 2 contractile vacuoles; pellicle and ectoplasm thick; conspicuous oesophageal fibrils beneath dorsal and right sides; in the stomach of cattle, sheep, goat, and reindeer (Awerinzew and Mutafowa, 1914). M. medium A. and M. (Fig. 349,/). 180-272/* by 111-175/*; in catsal
tle.

Genus Polyplastron Dogiel. Adoral and dorsal zones at anterior end; 2 skeletal plates beneath right surface, separate or fused; 3 longitudinal plates beneath left surface, with anterior ends connected by cross bars; contractile vacuoles beneath dorsal surface in a longitudinal row, also with additional vacuoles; in the stomach of cattle and sheep. Species (Kofoid and MacLennan, 1932).

SPIROTRICHA, OLIGOTRICHA
P. multivesiculatum (D. and Fedorowa) (Fig. 350,
78-140/*; in cattle
skeletal

821

a). 120-190/* by and sheep. MacLennan (1934) found that the plates are made up of small, roughly prismatic blocks of

glycogen, each with a central granule.

Genus Elytroplastron Kofoid and MacLennan. 2 zones

at anterior

end, 2 skeletal plates beneath right surface, a small plate beneath

troplastron

Polyplastron multivesiculatum, X360 (Dogiel); b, ElyX340 (Dogiel); c, Ostracodinium dentatum, X440 (Dogiel); d, Enoploplastron triloricatum, X370 (Dogiel); e, Epidinium caudatum, X340 (Becker and Talbott); f, E. ecaudatum, X340 (Becker and Talbott); g, Epiplastron africanum, X300 (Dogiel).
Fig. 350.
a,

hegneri,

ventral surface, and a long plate below left side; pellicle and ectoplasm thick; conspicuous fibrils beneath dorsal-right side. One
species.
b). 110-160/* by 67-97/*; and Bos indicus (Becker, 1933). Genus Ostracodinium Dogiel. 2 zones at anterior end; broad skeletal plate beneath right side 2-6 contractile vacuoles in a dorsal row
;

E. hegneri (Becker and Talbott) (Fig. 350,

in cattle, sheep, Buffelus bubalus

822

PROTOZOOLOGY
fibrils thick,

cytopharyngeal

extend to posterior end; in

cattle, sheep,

antelope, steenbok, and reindeer.

Numerous
c).

species (Kofoid

and
in

MacLennan,

1932).

0. dentatum (Fiorentini) (Fig. 350,

52-1

10/x

by 31-68 M

the stomach of cattle.

Genus Enoploplastron Kofoid and MacLennan. 2 zones near anterior

end; 3 skeletal plates beneath right- ventral side,

reindeer and antelope.

either

separate or partly fused; 2 contractile vacuoles; heavy pharyngeal

fibrils; in cattle,

E. triloricatum (Dogiel) (Fig. 350,

differences

among

d). Dogiel (1927) mentions size those occurring in different host species, as fol-

lows: in cattle, 85-1 12ju

in

by 51-7 0/x;
sp.),

in reindeer,

75-103^ by 40-58/x;

antelope (Rhaphiceros

60-110/x by 37-56/t.

Genus Epidinium Crawley. Elongate; twisted around the main

zone not at anterior end; 3 skeletal plates, with secondary plates; simple macronucleus club-shaped; 2 contractile vacuoles; in cattle, sheep, reindeer, camels, etc. Species (Kofoid and
axis; 2 zones; dorsal

MacLennan,

1932).
e).

E. caudatum (Fiorentini) (Fig. 350,

cattle, camels,

113 151/x by 45-61/z; in

Cervus canadensis and reindeer.

E. {Diplodinium) ecaudatum (F.) (Figs. 16; 350,

40-60/1 (Becker
classical

/). 112-140/x by and Talbott); in cattle, sheep, and reindeer. The observation of Sharp (1914) on its neuromotor system has

been described elsewhere

(p. 63).

Genus Epiplastron Kofoid and MacLennan. Elongate; 2 zones;

dorsal zone not at anterior end; 5 skeletal plates, with secondary
plates;

macronucleus simple, elongate; 2 contractile vacuoles; in

90-140**

antelopes.

E. africanum (Dogiel) (Fig. 350,

phiceros sp.

g).

by

30-55*t; in

Rha-

Genus Ophisthotrichum Buisson. 2 zones; dorsal zone

2 contractile vacuoles posterior; conjugation (Dogiel); in

at middle

or near posterior end of body; one-piece skeletal plate well developed;

many
by

Afri-

can antelopes. One species.

O.janus (Dogiel) (O. thomasi B.) (Fig. 351, Conjugation (Dogiel, 1925).

a).

90-150**

42-60*1.

Genus Cunhaia Hasselmann. Cytostome near anterior end, with

adoral zone; dorsal zone on 1/3 of anterior-dorsal surface; 2 contractile vacuoles; skeleton (?); in the

caecum

of guinea pig, Cavia

aperea.

One

species.

C. curvata

H.

(Fig. 351, b). 60-80**

by 30-40*t;

in Brazil.

SPIROTRICHA, OLIGOTRICHIA
Family 5 Cycloposthiidae Poche

823

and body rigid; zones of membranellae at anterior and posterior ends; more or less compressed; cytopharynx short and wide; macronucleus elongate; a single micronucleus; 2 or more contractile vacuoles; in horse and anthropoid apes. Genus Cycloposthium Bundle. Large, elongate barrel-shaped; cytostome in center of a retractile conical elevation at anterior end; adoral zone conspicuous; an open ring-zone of membranellae near posterior end on both dorsal and ventral sides; pellicle ridged; skelePellicle firm

Fig. 351. a, Ophisthotrichum janus, X370 (Dogiel); b, Cunhaia curvata, X670 (Hasselmann); c, Cycloposthium bipalmatum, X300 (Bundle); d, C. dentiferum, X270 (Hsiung), e, Spirodinium equi, X350 (Davis); f, Triadinium caudatum, X300 (Hsiung) g, T. minimum, X440 (Hsiung); h, Tetratoxum unifasciculatum, X280 (Hsiung).
;

824

PROTOZOOLOGY

ton club-shaped; several contractile vacuoles in a row along bandform macronucleus; in the caecum and colon of horse. Many species
(Hsiung, 1930). Cytology (Strelkow, 1929, 1932). C. bipalmatum (Fiorentini) (Fig. 351, c). 80-127/* by 35-57 /*. Conjugation (Dogiel, 1925).

Gassovsky (Fig. 351, d). 140-222/* by 80-110/*. Genus Spirodinium Fiorentini. Elongate, more or less fusiform; adoral zone at anterior end; anterior ciliary zone encircles the body
C. dentiferum at least once; a posterior ciliary arch, only 1/2 spiral; a dorsal cavity
of

unknown function

(Davis, 1941), lined with

stiff

rods; in the colon

and caecum

of the horse. Species (Hsiung, 1930, 1935).

S. equi F. (Fig. 351, e). 82-196/x by 46-108/*; widely distributed. Morphology (Hsiung, 1935a; Davis, 1941); division (Davis, 1941). Genus Triadinium Fiorentini. More or less helmet-shaped; compressed; adoral zone at anterior end; 2 posterior (ventral and dorsal) zones; with or without a caudal projection; in the caecum and colon
of horse. Species (Hsiung, 1935).

T.

caudatum F.

(Fig. 351,/). 59-86/*

by

50-68/*.

T. galea Gassovsky. 59-78/1

by

50-60/*.

T. minimum G. (Fig. 351, g). 35-58/* by 30-40/z. Genus Tetratoxum Gassovsky. Slightly compressed; 2 anterior and 2 posterior zones of membranellae in the colon of horse. Species
;

(Hsiung, 1930).
T. unifasciculatum (Fiorentini) (Fig. 351, h). 88-186/* by 60-108/*; widely distributed. Morphology and micronuclear division (Davis,

1941a).

by 55-90/*. parvum H. 67-98/* by 39-52/*. Genus Tripalmaria Gassovsky (Tricaudalia Buisson). Adoral zone at anterior end; 2 dorsal and 1 ventral-posterior zones in tuft-form;
T. escavatum Hsiung. 95-135/x T.

macronucleus inverted U-shape; in the colon of horse. Cytology

(Strelkow, 1932).
T. dogieli G. (Fig. 352, a). 77-123/* by 47-62/* (Hsiung, 1930). Genus Triplumaria Hoare. Adoral zone; 2 dorsal and 1 ventral cirrose tufts (caudals); skeleton, composed of polygonal plates arranged in a single layer, surrounds the body except the dorsal surface; dorsal groove supported by rod-like skeleton; macronucleus

elongate sausage-form, with a micronucleus attached to its dorsal surface near middle; about 6 contractile vacuoles arranged in line

along dorsal surface of body; in the intestine of Indian rhinoceros

(Hoare, 1937).
T. hamertoni

H. 129-207/* long, 65-82/*

thick, 4-39/* broad; endo-

SPIROTRICHA, OLIGOTRICHIA

825

Fig 352.

a,

Tripalmaria

dogieli,

periac'htum, X270 (Hsiung); c, d-f, Troglodytella abrassarti (d,

X180 (Gassovsky); b, Cochhatoxum Ditoxum funinucleum, X270 (Hsiung); X670 (Swezey); e, ventral and f, dorsal

view,

X210 (Brumpt and Joyeux)).

826

PROTOZOOLOGY

commensal in the intestine of Rhinoceros unicornis in Zoological Garden in London. Genus Cochliatoxum Gassovsky. Adoral zone near anterior end; 3 additional zones, 1 antero-dorsal, 1 postero-dorsal and 1 posteroventral; macro nucleus with curved anterior end; in the colon of
horse.

One species.
b).

C. periachtum G. (Fig. 352, 1930).

210-370/x by 130-210m (Hsiung,

2 dorsal (anterior

Genus Ditoxum Gassovsky. Large adoral zone near anterior end and posterior) zones; macronucleus curved club-

shaped; in the colon of horse (Hsiung, 1935). D.funinucleum G. (Fig. 352, c). 135-203^ by 70-101/x.

Genus Troglodytella Brumpt and Joyeux.

;

Ellipsoid;

flattened;

adoral zone 3 additional zones (anterior zone continuous or not con-

tinuous on ventral surface; posterior zone continuous on dorsal

surface;

between them a small zone on each

the colon of anthropoid apes.

side); skeletal plates in

anterior region; macronucleus L-form; contractile vacuoles in 2 circles; in

T. abrassarti B.
IGOyu;
in

and

J. (Fig.

352, d-f).

About 145-220/x by 120-

the colon of chimpanzees (Brumpt and Joyeux, 1912).

Reichenow (1920) distinguished var. acuminata on the basis of the drawn-out posterior end, which was found by Swezey (1932) to be a variant of T. abrassarti. Cytology (Swezey, 1934); cultivation (Nelson, 1932; Swezey, 1935). T. gorillae Reichenow. 200-280/z by 120-160/*; in the colon of
gorilla;

with anterior zone not reaching the right

side.

References

Awerinzew,

S.

and Mutafowa, R,: (1914) Material zur Kenntnis

der Infusorien aus dem Magen der Wiederkauer. Arch. Protist., 33:109. Balech, E.: (1942) Tintinnoineos del Estrecho le Maire. Physis, 19:
245. (1945) Tintinnoinea de Atlantida. Comm. Mus. Argent. Cien. Nat. Ser. Cien. Zool., no. 7. (1951) Nuevos datos aobre Tintinnoinea de Argentina y Uruguay. Physis, 20:291. Becker, E. R. (1933) Concerning Ehjtroplastron hegneri. Tr. Am.
:

Micr.Soc, 52:217. Schulz, J. A. and Emmerson, M. A. (1930) Experiments on the physiological relationships between the stomach Infusoria of ruminants and their hosts. Iowa State College J. Sc, 4:215. and Talbott, Mary: (1927) The protozoan fauna of the rumen and reticulum of American cattle. Ibid., 1:345.
,
:

SPIROTRICHA, OLIGOTRICHA
Bretschneider,

827

L. H.: (1934) Beitrage zur Strukturlehre der Ophryoscoleciden. II. Arch. Protist., 82:298. Brumpt, E. and Joyeux, C: (1912) Sur un infusoire nouveau parasite du Chimpanze, etc. Bull. Soc. Path. Exot., 5:499. Busch, W.: (1921) Studien iiber Ciliaten des nordatlantischen

Ozeans und Schwarzen Meers. I. Arch. Protist., 42:364. (1925) Beitrag zur Kenntnis der Gehausebildung bei den
Tintinnidae, etc. Ibid., 58:183.

Bush, Mildred and Kofoid, C. A.: (1948)

Ciliates

from the Sierra

Nevada bighorn, etc. Univ. California Publ. Zool., 53:237. Crawley, H.: (1923) Evolution in the ciliate family Ophryoscolecidae. Proc. Acad. Nat. Sc. Philadelphia, 75:393. da Cunha, A. M.: (1914) Ueber die Ziliaten, welche in Brasilien im Magen von Rindern und Schafen vorkommen. Mem. Inst. Oswaldo Cruz., 6:58. (1917) Sobre os ciliados do tubo digestivo dos mammideros. Buenos Aires. 8 pp. Das-Gupta, M.: (1935) Preliminary observations on the protozoan fauna of the rumen of the Indian goat, etc. Arch. Protist., 85:
153.

Davis, T. G.: (1941) Morphology and division J. Morphol., 69:225.

in

Spirodinium

equi.

(1941a) Morphology and division in Tetratoxum unifasciculatum. Tr. Am. Micr. Soc, 60:441. Dogiel, V.: (1925) Die Geschlechtsprozesse bei Infusorien, etc. Arch. Protist., 50:283. (1927) Morphologie der Familie Ophryoscolecidae. Ibid., 59:1. (1932) Beschreibung einiger neuer Vertreter der Familie Ophryoscolecidae, etc. Ibid., 77:92. (1934) Angaben liber die Ophryoscolecidae, etc. Ibid., 82: 290. and Fedorowa, T. (1929) Ueber die Zahl der Infusorien im Wiederkauermagen. Zentralbl. Bakt. I. Orig., 112:135. Ferber, K. E. and Fedorowa, T.: (1929) Zahlung und Teilungsquote der Infusorien im Pansen der Wiederkauer. Biol. Zentralbl., 49:321. Fernandez, D. F.-G.: (1949) Sobre el aparato neuromotor y otras estructuras protoplasmaticas de "Ophryoscolex purkinjei." Trab. Inst. Cien. Nat. J. d. Acosta, 2:257. Hoare, C. A.: (1937) A new cycloposthiid ciliate, etc. Parasitology, 29:559. Hofker, J.: (1932) Studien liber Tintinnoidea. Arch. Protist., 75: 315. Hsiung, T. S.: (1930) A monograph on the Protozoa of the large intestine of the horse. Iowa State College J. Sc, 4:356. (1935) Notes on the known species of Triadinium, etc Bull. Fan Mem. Inst. Biol., 6:21. (1935a) On some new ciliates from the mule, etc. Ibid., 6:81. Kahl, A.: (1932) Urtiere oder Protozoa. I. Dahl's Die Tierwelt
:

Deutschlands,

etc.

Part 25.

828

PROTOZOOLOGY

in the evolution of the pelagic ciliata, the Tintinnoinea. Contr. Marine Biol., Stanford Univ., 39 pp. and Campbell, A. S.: (1929) A conspectus of the marine and freshwater Ciliata, belonging to the suborder Tintinnoinea, etc. Univ. California Publ. Zool., 34:1. and Christenson, J. F.: (1934) Ciliates from Bos gaurus. Ibid., 39:341. and MacLennan, R. F.: (1930) Ciliates from Bos indicus I. Ibid., 33:471. Ibid., 37 53. (1932) II. (1933)111. Ibid., 39:1. MacLennan, R. F.: (1933) The pulsatory cycles of the contractile vacuoles in the Ophryoscolecidae, etc. Ibid., 39 205. (1935) Ciliates from the stomach of musk-deer. Tr. Am. Micr. Soc, 54:181. Mowry, Helen A. and Becker, E. R.: (1930) Experiments on the biology of Infusoria inhabiting the rumen of goats. Iowa State College J. Sc, 5:35. Nelson, E. C: (1932) The cultivation of a species of Troglodytella, etc. Science, 75:317. Rampi, L.: (1950) I Tintinnoidi della acque di Monaco, etc. Bull. l'lnst. OcSanogr., no. 965. Reichenow, E.: (1920) Den Wiederkauer-Infusorien verwandte Formen aus Gorilla und Schimpanse. Arch. Protist., 41:1. Silva, Estela de S. E. (1950) Les Tintinnides de la baie de Cascais (Portugal). Bull. PInst. Oc6anogr., no. 974. Strelkow, A.: (1929) Morphologische Studien iiber oligotriche Infusorien aus dem Darme des Pferdes. I. Arch. Protist., 68:503. (1932) II, III. Ibid., 75:191.
:
: :

Kofoid, C. A.: (1930) Factors

Swezey, W. W.: (1932) The transition

sitol.,

of Troglodytella abrassarti and T. a. acuminata, intestinal ciliates of the chimpanzee. J. Para-

19:12. (1934) Cytology of Troglodytella abrassarti, etc. J. Morphol.,

56:621. (1935) Cultivation of Troglodytella abrassarti, etc. J. Parasitol., 21:10. Szabo, M.: (1935) Neuere Beitrage zur Kenntnis der Gattung Halteria. Arch. Protist., 86:307.

Chapter 40

Order 2 Spirotricha Blitschli (continued)

Suborder 3 Ctenostomata Lauterborn
placed group THE forms with a very sparse
ciliates

in this

are carapaced

and compressed
is

ciliation.

The

adoral zone

also re-

duced to about 8 membranellae. These organisms are exclusively free living and sapropelic in fresh, brackish, or salt water. Morphology and taxonomy (Kahl).
Posterior half of carapace with 4 ciliated rows on left and at least 2 rows on right; with anterior row of cilia on left side. .Family 1 Epalcidae Posterior half of carapace with cirrus-like groups on left only, none on right; without frontal cilia

Long

ciliated

band extends over both broad

sides

Short ciliated

Family 2 Discomorphidae band ventral, extending equally on both broad sides. Family 3 Mylestomidae (p. 830)
.

Family

Epalcidae Wetzel

triangular; anterior end pointed toward ventral surface, posterior end irregularly truncate; dorsal surface more convex; right carapace with 1 dorsal and 1 ventral ciliary row in posterior region; usually 4 (2-3) median teeth; all anal teeth without spine with comb-like structures posterior to oral aper;

Genus Epalxis Roux. Rounded

ture; 1-2 oval macronuclei dorsal; contractile vacuole posterior-

ventral; sapropelic in fresh or salt water.

Many species.

E. mirabilis R. (Fig. 353, a). 38-45/* by 27-30/*; fresh water. Genus Saprodinium Lauterborn. Similar to Epalxis; but some (left and right) of anal teeth with spines; sapropelic in fresh or salt
water. Several species.
S. dentatum L. (Fig. 353, b). 60-80/* long; fresh

water (Lackey,

1925).
S.

putrinium Lackey (Fig. 353,

;

c). 50/t

long, 40/z wide,

about

15/i

thick in Imhoff tanks.

Genus Pelodinium Lauterborn. Right carapace with 2 median rows of cilia, its median anal teeth fused into one so that there are only three teeth. One species.
P. reniforme L. (Fig. 353, d). 40-50/t long; sapropelic.

Family 2 Discomorphidae Poche

Genus Discomorpha Levander. Oval; ventrally directed anterior

spine long; posterior end without teeth or ridges; ciliated bands on

829

830

PROTOZOOLOGY

Fig. 353. a, Epalxis mirabilis, X1200 (Roux); b, Saprodinium dentatum, X430 (Kahl); c, S. pulrinium, X470 (Lackey); d, Pelodinium reniforme, X600 (Lauterborn); e, f, Discomorpha pectinata, (e, X500; f, X220) (Kahl); g, Mylestoma bipartitum, X470 (Kahl); h, Atopodinium fibulatum, X520 (Kahl).

posterior-left; sapropelic.

both lateral surfaces; 2 spines on right side; 2 cirrus-like groups on A few species. D. pectinata L. (Fig. 353, e,f). 70-90/* long; sapropelic.

Family 3 Mylestomidae Kahl

tion,

Genus Mylestoma Kahl. Posterior margin without any indentathough sometimes a small one on right side, but none on left;

SPIROTRICHA, CTENOSTOMATA

831

3 often long ribbon-like cirri on peristome; fresh or salt water. Several species.

bipartitum (Gourret and Roesner) (Fig. 353, g). 35-50/z long; two caudal processes; salt water. Genus Atopodinium Kahl. Posterior left side with one large, and right side with 2 indentations; macronucleus spherical; sapropelic. A.fibulatum K. (Fig. 353, h). 4O-50m long.
.

References

Kahl,

A.: (1932) Ctenostomata (Lauterborn) n. Subord. Arch. Pro-

tist.,

77:231. (1932a) Urtiere oder Protozoa. Dahl's Die Tierwelt Deutsch-

Lackey,

lands, etc. Part 25. J. B.: (1925) Studies on the biology of sewage disposal. The fauna of Imhoff tanks. Bull. New Jersey Agric. Exper. Station, no. 417.

Chapter

41

Order 2 Spirotricha

Blitschli (continued)

Suborder 4 Hypotricha Stein

THE
cilia

members

of this suborder are, as a rule, flattened

and strong

or cirri are restricted to the ventral surface. Except the fam-

ily

Aspidiscidae, the dorsal surface possesses rows of short slightly

tactile bristles.

moveable

The peristome
cirri

is

very large with a wellcalled,

developed adoral zone. The

on the ventral surface are

according to their location, frontals, ventrals, marginals, anals (transversals), and caudals, as was mentioned before (Fig. 11, b).

Asexual reporduction

is

conjugation. Encystment

by binary fission and sexual reproduction by is common. Mostly free-living in fresh,

brackish or salt water; a few parasitic.

Adoral zone fully formed Cirri on ventral surface Ventrals in rows, though in some reduced; 2 rows of marginals. Family 1 Oxytrichidae Ventrals and marginals not in longitudinal rows Family 2 Euplotidae (p. 839) Family 3 Paraeuplotidae (p. 843) No ventral cirri; caudal cirri Family 4 Aspidiscidae (p. 845) Adoral zone reduced
.

Family

Oxytrichidae Kent
Sterki; Opisthotricha

Genus Oxytricha Ehrenberg (Histrio

Kent;

Steinia Diesing). Ellipsoid; flexible; ventral surface flattened, dorsal

surface convex; 8 frontals; 5 ventrals; 5 anals; short caudals; marginals

may

or

may

not be continuous along posterior border; macro-

nucleus in 2 parts, rarely single or in 4 parts; fresh or salt water. Numerous species (Horvath, 1933); neuromotor system (Lund,
1935). 0. fallax Stein (Fig. 354, a). Posterior region broadly rounded; about 150^ long; fresh water. Amicronucleate race (Reynolds, 1932). 0. bifaria Stokes (Fig. 354, b). Right side convex; left side flattened; posterior end pointed; about 250m long; fresh water infusion. 0. ludibunda S. (Fig. 354, c). Ellipsoid; flexible; 100m long; fresh water among sphagnum. O. setigera S. (Fig. 354, d). Elongate ellipsoid; 5 frontals; ventrals
shifted anteriorly; 50m long; fresh water. Genus Tachysoma Stokes (Actinotricha Cohn). Flexible; frontals

8-10, of which anterior three are usually the largest; 5 ventrals

832

SPIROTRICHA, HYPOTRICHA
scattered; 5 anals; marginals at
;

833
lateral borders,

some distance from

interrupted posteriorly fresh or salt water.

T. parvistyla S. (Fig. 354, e). 10 frontals scattered; about 63 n long;
in shallow freshwater pools.

Genus Urosoma Kowalewski. Similar

portion drawn out and

to Oxytricha; but posterior

much narrowed

fresh water.

U. caudata (Stokes) (Fig. 354, /). 200-250/1 long; pond water. Genus Amphisiella Gourret and Roeser. With a single row of ventrals and 2 marginal rows; salt or fresh water. Several species.

A. thiophaga (Kahl) (Fig. 354,

g).

70-100^ long;

salt water.

Genus Eschaneustyla Stokes.

Elliptical or ovate;

narrow

peri-

c,

Fig. 354. a, Oxytricha fallax, X230 (Stein); b, O. bifaria, X180 (Stokes); O. ludibunda, X400 (Stokes); d, O. setigera, XS70 (Stokes); e, Tachysoma parvistyla, X490 (Stokes); f, Urosoma caudata, X250 (Stokes);
g,

Amphisiella thiophaga,

(Stokes); i, cycliostyla sphagni, X300) (Kahl). 1,

X240

X380 (Kahl); h, Eschaneustyla brachytona, Gonostomum strenuum, X160 (Engelmann) ],HemiX100 (Stokes); k, 1, Cladotricha koltzowii (k, X170;
;

834

PROTOZOOLOGY

to 2 at anterior margin; ventrals small

stome 1/3 the body length; frontals numerous, about 22 in addition and numerous in 3 oblique rows; no anals; marginals uninterrupted; contractile vacuole a long
canal near
left

border; fresh water.

S. (Fig.

One

species.

E. brachytona

354, h). 170-220/* long.

Genus Gonostomum Sterki (Plagiotricha Kent). Flexible; 8 or more frontals; 1-2 oblique ventral rows of short cirri; 4 or 5 anals; 2
marginal rows; fresh water.
G. strenuum
bristles;

(Engelmann)

(Fig. 354,

i).

Elongate; with caudal

about

150/t long; fresh water.

Genus Hemicycliostyla Stokes. Elongate oval; flexible; ends rounded; 20 or more frontals, arranged in 2 semicircular rows; adoral row begins near center on right side of peristomal field; ventral surface entirely covered with fine cilia; no anals; one or more contractile vacuoles nucleus distributed fresh water. H. sphagni S. (Fig. 354, j). About 400-500/* long; marsh water
;

with sphagnum. Genus Hypotrichidium Ilowaisky. Two ventral and marginal rows of cirri spirally arranged; peristome large, extends 1/2 the body length, with a large undulating membrane; 2 macro- and micro-nuclei;

contractile vacuole anterior-left; fresh water.

I.

H. conicum

(Fig. 355, a).

90-1 50/* long.

Genus Cladotricha Gajevskaja. Elongate band-form; anterior

featherly

end rounded, posterior end rounded or attenuated; frontals only 2 cirri; macronucleus spheroidal; micronucleus; without contractile vacuole; salt water, with 5-20 per cent salt content. One
species.

C. koltzowii G. (Fig. 354, k,

posteriorly attenuated forms

Genus

Psilotricha Stein.

I). Band-form up to about 200/* long; up to about 100/* long. Oval to ellipsoid; frontals and anals un-

differentiated; ventrals

and marginals long cirri, few; ventrals in 2 rows and a rudimentary row toward left; with or without zoochlorellae; fresh water. A few species. P. acuminata S. (Fig. 355, 6). 80-100/* long. Genus Kahlia Horvath. Frontal margin with 3-4 strong cirri; 5-8 ventral longitudinal rows marginals sapropelic in fresh water. K. acrobates H. (Fig. 355, c). 100-200/x long; soil infusion. Genus Uroleptus Ehrenberg. Elongate body drawn out into a taillike portion; 3 frontals; 2-4 rows of ventral cirri; marginals; no anals; sometimes rose- or violet-colored; fresh or salt water. Many
; ;

species.

among

U. limnetis Stokes (Fig. 355, d). vegetation.

About

200/x long; fresh

water

SPIROTRICHA, HYPOTRICHA
U. longicaudatus S. (Fig. 355,
e).

S3 5

About

200/* long;

marsh water

with sphagnum. U. halseyi Calkins (Fig. 355,/). About 160/t by 20/*; peristome 1/6-1/7 the body length; 3 ventrals; macronucleus divided into many (up to 26) parts; 2 (1-3) micronuclei; fresh water (Calkins,
1930).

Genus Uroleptopsis Kahl. Ventrals

water.

in 2 uninterrupted rows; salt

A few

species.

Fig. 355. a, Hypotrichidium conicum, X200 (Kahl); b, Psilotricha acuminata, X230 (Stein); c, Kahlia acrobates, X240 (Kahl); d, Uroleptus limnetis, X240 (Stokes); e, U. longicaudatus, X240 (Stokes); f, U. halseyi, X470 (Calkins); g, Uroleptopsis citrina, X260 (Kahl); h, Strongylidium califor nicum, X200 (Kahl); i, Stichotricha secunda, X340 (Kahl); j, S. intermedia (Froud); k, Chaetospira mulleri (Froud); 1, Urostyla grandis, X140 (Stein); m, U. trichogaster, XI 50 (Kahl).

836

PROTOZOOLOGY

U. citrina K. (Fig. 355, g). Elongate; flexible; ectoplasm with pale-yellow ringed bodies which give the organism yellowish color;

marginals discontinuous posteriorly; 2 contractile vacuoles near

left

border; 150-25CV long; salt water.

Sterki. 2-5 ventral rows of cirri; marginals 3-6 frontals; 2 or more macro nuclei; fresh or salt

Genus Strongylidium
spirally arranged;

water.

Many

species.

Kahl (Fig. 355, h). 4-5 frontals; macronuclei about 30 in number; 4 micronuclei; contractile vacuole with short canals; about 250/* long; fresh water among vegetation.
S. californicum

Genus Stichotricha Perty. Slender ovoid or fusiform; peristomebearing part narrowed; not flexible; usually 4 spiral rows of
cirri;

sometimes tube-dwelling, and then

in groups; fresh or salt water.

Many

species.
i).

S. secunda P. (Fig. 355, S. intermedia

130-200/i long; in fresh water.

-

long, 2/5 of rows of dorsal

Froud (Fig. 355, J )- Solitary; non-loricate; 40-170/x which is a bent proboscis; two rows of body cilia; two
cilia, 5/t

long;

among Lemna

in fresh

water (Froud,

1949).

Genus Chaetospira Lachmann. Similar

stome-bearing part

to Stichotricha;

but peri-

flexible; fresh or salt water.

C. mulleri L. (Fig. 355, k). Flask-shaped, 60-200 /i long, in a lorica; cytostome at the base of proboscis; a single (two or more) micronucleus; macronucleus in two to eight parts; ingested diatoms lose color in 10 minutes; Bodo is immobilized in less than one minute; binary fission; the anterior individual remains in the lorica, while the posterior individual (averaging 46 /i long) swims away and sooner or later becomes attached to substrate; cysts pyriform, 35-55/x by 15-20/i among Lemna in fresh water (Froud, 1949).
;

ends rounded; and 2 marginal rows; 3 or more frontals; 5-12 anals; macronucleus a single
Ellipsoid;
flexible;

Genus Urostyla Ehrenberg.

flattened ventral surface with 4-10 rows of small cirri

body or in many

parts; fresh or salt water.

I).

Numerous

species.

U. grandis E. (Figs. 49; 355,

1946, 1947) (p. 165).

300-400/t long; macronucleus in

100 or more parts; 6-8 micronuclei; fresh water. Nuclei (Raabe,

U. trichogaster Stokes (Fig. 355, m). 250-330/t long; fresh water.

U. caudata S. (Fig. 356, a). Elongate ellipsoid; flexible; narrowed anterior part bent to left; peristome 1/3 the body length; macronucleus in many parts; contractile vacuoles near left margin; about
600/* long; fresh

water with sphagnum.

SPIROTRICHA, HYPOTRICHA

837

U. pohjmicronucleata Merriman. Elliptical with broadly rounded

ends; flexible; 225m by 65m; opaque, green or brown because of the ingested diatoms; 3 large and 10 small frontals; four ventral rows of

marginals; macronucleus in two parts; three to 11 micronuclei (Merriman, 1937). U. coei Turner. Elliptical, with a more pointed posterior end; 200 m by 50m; four rows of ventral cirri, the right row being the longest; five frontals; macronucleus in two masses; four micronuclei (Turner,
cirri;

1939).

of ventral cirri;

Genus Kerona Ehrenberg. Reniform; no caudals; 6 oblique rows commensal. One species.

Fig. 356. a, Urostyla caudata, X90 (Stokes); b, Kerona polyporum, X200 (Stein); c, Keronopsis rubra, X270 (Entz); d, Epiclintes pluvialis, XlOO (Smith); e, Holosticha vernalis, X220 (Stokes); f, H. hymenophora, XlSO (Stokes); g, Paraholosticha herbicola, X200 (Kahl); h, Trichotaxis stagnatilis, X190 (Stokes); i, Balladyna elongata, X800 (Roux); j, Pleurotricha lanceolata, X250 (Stein); k, Gastrostyla muscorum, X200 (Kahl).

838

PROTOZOOLOGY

K. polyporum E. (Fig. 356, b). 120-200/* long; commensal on Hydra. Genus Keronopsis Penard. Two ventral rows of cirri reaching frontal field; caudals variable; macro nucleus usually in several
(rarely 2) parts; fresh or salt water.

Numerous

species.
salt

K. rubra (Ehrenberg)
water.

(Fig. 356, c).

Reddish; 200-300/* long;

Genus

Epiclintes Stein. Elongate; spoon-shaped; flattened ven-

tral surface

with more than 2 rows of

d).

cirri;

2 marginal rows; frontals

undifferentiated; anals; no caudals; salt or fresh water.

A few species.

E. pluvialis Smith (Fig. 356,

About 375m long;

fresh water.

Genus Holosticha Wrzesniowski. Three frontals along anterior margin; 2 ventral and 2 marginal rows of cirri; anals; fresh or salt
water.

Numerous

species.

H. vernalis Stokes (Fig. 356, e). 7 anals; about 180/z long; shallow pools with algae. H. hymenophora S. (Fig. 356,/). 5 anals; 2 contractile vacuoles;
160-200/1 long; shallow pools.

in

Genus Paraholosticha Kahl. Elongate-oval; flexible; ventral cirri 2 parallel oblique rows; with a row of stiff cirri along frontal marit

gin, posterior to

2 short rows of

cirri;

marginals continuous or

interrupted at posterior border; fresh water.

P. herbicola K. (Fig. 356,

algae.

g).

150-190/t long; fresh water

among

Genus Trichotaxis Stokes. Similar

of ventral cirri; fresh or salt water.

to Holosticha; but with 3 rows

T. stagnatilis S. (Fig. 356, h).

About

160/t long; ellipsoid; in fresh

water among decaying vegetation. Genus Balladyna Kowalewski. Ellipsoid; frontals not well developed or lacking; 1 ventral and 2 marginal rows of cirri; long
dorsal and lateral
stiff cirri;

fresh water.
i).

B. elongata

Roux

(Fig. 356,

32-35/t

by

11-12/*; fresh

water

among

plants and detritus.

Stein.

Genus Pleurotricha
2 rows of ventral

Oblong to

ellipsoid;

marginals continu-

ous; 8 frontals; 3-4 ventrals; 7 anals of which 2 are

cirri;

more

posterior;

between ventrals and marginals 1-3 rows of

few coarse

cilia;

fresh water.

P. lanceolata (Ehrenberg) (Fig. 356, j). 100-165/* long; 2 macroand 2 micro-nuclei. Manwell (1928) studied its conjugation, division,

encystment and nuclear variation. Encystment (Penn, 1935). Genus Gastrostyla Engelmann. Frontals distributed except 3 along the frontal margin; ventrals irregular; 5 anals; macronucleus divided

SPIROTRICHA, HYPOTRICHA
into 2-8 parts; fresh or salt water.

839

Morphology and physiology

(Weyer, 1930).
G.

muscorum Kahl

(Fig. 356, k).

130-200^ long; macronucleus in

to reniform; not flexible;

8 parts; fresh water in vegetation.

Genus Stylonychia Ehrenberg. Ovoid

ventral surface
flat,

dorsal surface convex; 8 frontals; 5 ventrals;

5 anals; marginals; 3 caudals; with short dorsal bristles; fresh or salt

water.

Many

species.

S. mytilus (Muller) (Fig. 357, a).

100-30(V long; fresh, brackish

and

Encystment (von Brand, 1923). S. pustulata E. (Figs. 93; 357, b). About 150/j, long; fresh water. Cytology (Hall, 1931) division and reorganization (Summers, 1935).
salt water.
;

S. putrina Stokes (Fig. 357,

c).

125-150/x long; fresh water.

S. notophora S. (Fig. 357, d).

About 125^ long; standing water. Genus Onychodromus Stein. Not flexible; somewhat rectangular;
flat,

anterior end truncate, posterior end rounded; ventral surface

3 frontals; 3

dorsal surface convex; peristome broadly triangular in ventral view;

rows of

cirri parallel to

the right edge of peristome; 5-6

anals; marginals uninterrupted; 4-8 macronuclei; contractile vacuole; fresh water.

One species.
e).

0. grandis S. (Fig. 357,

100-300^ long.

Genus Onychodromopsis Stokes. Similar

flexible; 6 frontals of

to Onychodromus; but which the anterior three are the largest; fresh

water.

One

species.

O.flexilis S. (Fig. 357,/). 90-125/z long; standing

pond water.

Family 2 Euplotidae Claus

Genus Euplotes Ehrenberg.

Inflexible

body ovoid; ventral surface

lies in flat

flattened, dorsal surface convex; longitudinally ridged; peristome

broadly triangular; frontal part of adoral zone

or

furrow; 9

more

frontal- ventrals; 5 anals; 4 scattered caudals; macronucleus

band-like; a micronucleus; contractile vacuole posterior; fresh or

salt water.

Many

species.

Comparative morphology (Pierson, 1943).

;

E. patella (Muller) (Fig. 357, g). Subcircular to elliptical; average dimensions 91^ by 52^; 9 f rontal-ventrals aboral surface with 6 pro-

minent ridges with rows of bristles embedded in rosettes of granules; peristome narrow; peristomal plate small triangle; macronucleus simple C-form band; micronucleus near anterior-left end; membranellae straight; posterior end of cytopharynx anterior to, and to left of, the fifth anal cirrus; post-pharyngeal sac; fresh and brackish water. Doubles and amicronucleates (Kimball, 1941) mating types
;

(p. 194).

840

PROTOZOOLOGY

Fig. 357.

a,

(Roux);

c,

S. putrina,

Stylonychia mytilus, X200 (Stein); b, S. pustulata, X400 X200 (Stokes); d, S. notophora, X200 (Stokes); e,
(Stein);
f,

Onychodromus grandis, X230

Onychodromopsis

flexilis,

X240

(Stokes); g, Euplotes patella, X420 (Pierson); h, E. eurystomus, X330 (Pierson); i, E. woodruffi,, X310 (Pierson); j, E. aediculatus, X290 (Pierson).

SPIROTRICHA, HYPOTRICHA
length 100-195/*; average dimensions 138/* by
;

841

E. eurystomus Wrzesniowski (Fig. 357, h). Elongated ellipsoid;

78/*;

9 f rontal-ventrals
;

no aboral ridges, but 7 rows of bristles peristome wide, deep peristomal depression sigmoid; membranellae forming sigmoid curve; end of cytopharynx far to left and anterior to the fifth anal cirrus; post-pharyngeal sac; macronucleus 3-shaped; micronucleus near flattened anterior corner of macronucleus; fresh and brackish water. Division and conjugation (Turner, 1930); neuromotor system (Turner, 1933; Hammond, 1937; Hammond and Kofoid, 1937).
E. woodruffi Gaw (Fig. 357, i). Oval; length 120-165/*; average dimensions 140/1 by 90/*; 9 f rontal-ventrals aboral surface often with 8 low ridges; peristome wide, with a small peristomal plate; end of cytopharynx almost below the median ridge; 4th ridge between
;

cirri often extends to anterior end of body; post-pharyngeal sac; macronucleus consistently T-shaped; micronucleus anterior-right; brackish (with salinity 2.30 parts of salt per 1000) and fresh water (Gaw, 1939).

anal

E. aediculatus Pierson (Fig. 357, average dimensions 132/* by 84/*; 9

j). Elliptical;

length 110-165/*;
;

f rontal-ventrals

aboral surface

usually without ridges, but with about 6 rows of bristles; peristome

narrow; peristomal plate long triangular, drawn out posteriorly; a niche midway on the right border of peristome; anal cirri often form
a straight transverse line; 4th ridge between anals may reach anterior end of body; macronucleus C-shape with a flattened part in the leftanterior region; micronucleus some distance from macronucleus at anterior-left region; post-pharyngeal sac; fresh and brackish (salinity 2.30 parts of salt per 1000) water.

E. plumipes Stokes. Similar to E. eurystomus. About 125/* long;

fresh water.

E. carinatus S. (Fig. 358,

a).

About
b).

70/*

by

50/*; fresh

water.

E. charon (Miiller) (Fig. 358,

70-90/* long; salt water.

Genus Euplotidium Noland. Cylindrical; 9 f rontal-ventrals in 2 rows toward right; 5 anals; a groove extends backward from oral region to ventral side, in which the left-most anal cirrus lies; peristome opened widely at anterior end, but covered posteriorly by a transparent, curved, flap-like membrane; adoral zone made up of about 80 membranellae; longitudinal ridges (carinae), 3 dorsal and 2 lateral; a row of protrichocysts under each carina; a broad zone of protrichocysts in antero-dorsal region; cytoplasm densely granulated; salt water. One species (Noland, 1937). E. agitatum N. (Fig. 358, c, d). 65-95/* long; erratic movement rapid; observed in half-dead sponges in Florida.

842

PROTOZOOLOGY

Fig. 358.

a,

Euplotes carinatus,

X430

(Stokes); b, E. charon,

X440

Euplotidium agitatum, X540 (Noland); e, Certesia quadrinucleata, X670 (Sauerbrey); f, Diophrys appendiculata, X570 (Wallengren); g, Uronychia setigera, X870 (Calkins); h, Aspidisca X300 (Stein); i, A. polystyla, X290 (Kahl).
(Kahl);
c,

d,

SPIROTRICHA, HYPOTRICHA
Genus Certesia Fabre-Domergue.
Ellipsoid; flattened;

843
dorsal

surface slightly convex, ventral surface flat or concave; 5 frontals

at anterior border; 7 ventrals; 5 anals; no caudals; marginals small
in

number; 4 macronuclei;
C.

salt water.

One
e).

species.

quadrinucleata F.-D. (Fig. 358,

70-100m by about
relatively
large,

45/i.

Morphology (Sauerbrey, 1928). Genus Diophrys Dujardin. Peristome

often

reaching anals; 7-9 frontal-ventrals; 5 anals; 3 strong dorsal near posterior margin; salt water.

cirri right-

water;

D. appendiculata (Ehrenberg) (Fig. 358, /). 60-lOOyu long; salt Woods Hole (Calkins). Division and reorganization (SumStein.

mers, 1935).

Genus Uronychia

Without frontals and ventrals; 5 anals;

a large undulating
g). 40/z

3 right-dorsal cirri (as in Diophrys); 2 left-ventral cirri near posterior

margin; peristome, oval with

U. setigera Calkins (Fig. 358,
Hole.

membrane on
water;

right edge; salt water. Several species.

by

25/z; salt

Woods

Genus Gastrocirrhus
cilia;

Lepsi. Anterior

end truncate with a ring of

posterior end bluntly pointed; slightly flattened; a wide peri-

stome leading to cytostome, with undulating membrane on left; 16 cirri on ventral surface arranged on right and posterior margins
(Lepsi) or six frontals, five ventrals, five caudals (Bullington)
rine.
;

ma-

Apparently intermediate between Heterotricha and Hypo-

tricha (Lepsi). G. stentoreus Bullington (Fig. 359, a). About 104^ by 71-8 1/t; dark granulated cytoplasm; active jumping as well as swimming move-

ment;

in

Tortugas (Bullington, 1940).

Family 3 Paraeuplotidae Wichterman

Genus Paraeuplotes Wichterman. Ovoid; ventral surface slightly concave, dorsal surface highly convex and bare, but with one ridge; frontal and adoral zones well developed ventral surface with a semicircular ciliary ring on the right half, posterior half of which is marked by a plate and with two ciliary tufts, near the middle of an;

5-6 caudal cirri; macronucleus curved band-form; a terminal contractile vacuole; zooxanthellae, but no food vacuole in cytoplasm; marine, on the coral.
terior half;

P. tortugensis
individuals 85/z

W.
by

(Fig. 359,
75/x;

b,

c).

Subcircular to ovoid; average

ciliary plate

37

/jl

long, with longer cilia;

adoral zone reaches nearly the posterior end; "micronucleus not clearly differentiated" (Wichterman); 5-6 caudal cirri about 13/*

844

PROTOZOOLOGY
fill

long; zooxanthellae yellowish brown, about 12 p. in diameter,

the

body; found on Eunicea crassa (coral); Tortugas, Florida. Genus Euplotaspis Chatton and Seguela. Ellipsoid; ventral surface flat or slightly concave; dorsal surface convex; membranellae and cirri with fringed tips; peristome very long; 10 frontal-ventrals; five
anals; three or four caudals difficult to see in
life;

dorsal surface

without striae or

macronucleus arched band; a single micronucleus. One species (Chatton and Seguela, 1936).
ciliary processes;

-^

Fig. 359.

a,

ventral view of Gastrocirrhus stenloreus,

X330

(Bullington)

(ac, anterior cirri; cc,

caudal

cirri; cp,
c,

cytopharynx;

oc, oral cilia;

om,

oral

membrane;

vc, ventral cirri); b,

dorsal

and ventral views

of Paraeu-

plotes tortugensis,

X490 (Wichterman)

(avc, anterior ventral cilia; cp,

ciliary plate; cpc, ciliary plate cilia; cv, contractile vacuole; ds, dorsal

swelling; fm, frontal membranellae;

cirri; te, tufts of cilia; zo,

cionaecola,

X1285

om, adoral membranellae; sp. caudal zoothanthellae) d, ventral view of Euplotaspis (Chatton and Seguela).
;

SPIROTRICHA, HYPOTRICHA

845

E. cionaecola C. and S. (Fig. 359, d). 60-70 m by 45-55m; in the branchial cavity of the ascidian, Ciona intestinalis.

Family 4 Aspidiscidae Claus

Genus Aspidisca Ehrenberg. Small; ovoid;

;

inflexible; right

and

dorsal side convex, ventral side flattened; dorsal surface conspicu-

ously ridged ado ral zone reduced or rudimentary 7 frontal-ventrals;

;

5-12 anals; macronucleus horseshoe-shaped or occasionally in 2 rounded parts; contractile vacuole posterior; fresh or salt water.

Numerous

species.
h).

A. lynceus E. (Figs. 55; 358,

30-50/x long; fresh water. Division

and reorganization (Summers, 1935). A. polystyla Stein (Fig. 358, i). About Hole (Calkins).
References

50/x long;

marine;

Woods

Bullington, W. E. (1940) Some ciliates from Tortugas. Carnegie Inst. Wash. Publ. no. 517. Calkins, G. N.: (1902) Marine Protozoa from Woods Hole. Bull.
:

Fish Comm, 21:415. U. (1930) Uroleptus

S.

halseyi. II. Arch. Protist., 69:151.

la
etc. Bull. soc. zool.

Chatton, E. and Segtjela, Josephine: (1936) Un hypotriche de

branchie de Ciona intestinalis,
232.

France, 61

Froud, Joan: (1949) Observations on hypotrichous ciliates: the genera Stichotricha and Chaetospira. Quart. J. Micr. Sc, 90:
141.

Gaw, H.

Hall, R.

Arch. Protist., 93 1. (1939) Euplotes woodruffi sp. n. Vacuome and Golgi apparatus in the ciliate, Stylonychia. Ztschr. Zellforsch. mikr. Anat., 13:770. Hammond, D. M.: (1937) The neuromotor system of Euplotes patella during binary fission and conjugation. Quart. J. Micr. Sc, 79:507. and Kofoid, C. A.: (1937) The continuity of structure and function in the neuromotor system of Euplotes patella, etc. Proc. Am. Philos. Soc, 77:207. Horvath, J. v.: (1933) Beitrage zur hypotrichen Fauna der Umgebung von Szeged. I. Arch. Protist., 80:281. Kent, S.: (1881-1882) A manual of Infusoria. London. Lepsi, J.: (1928) Un nouveau protozoaire marine: Gastrocirrhus inAnn. Protistologie, 1 195. termedius. Lund, E. E.: (1935) The neuromotor system of Oxytricha. J. Morphol., 58:257. Manwell, R. D.: (1928) Conjugation, division and encystment in Pleurotricha lanceolata. Biol. Bull., 54:417. Merriman, D.: (1937) Description of Urostyla poly micr onucleata. Arch. Protist., 88:427.
Z.
:

P.: (1931)

846

PROTOZOOLOGY

Noland,

L. E.: (1937) Observations on marine ciliates of the Gulf coast of Florida. Tr. Am. Micr. Soc, 56:160. Penn, A. B. K: (1935) Factors which control encystment in Pleurotricha lanceolata. Arch. Protist., 84:101. comparative morphological study Pierson, Bernice F.: (1943) J. Morphol., 72: 125. of several species of Euplotes, etc. Raabe, H.: (1946) L'appareil nucleaire d'Urostyla grandis. I. Ann. Uni. Marie Curie-Sklodowska, 1:1. Ibid., 1:133. (1947) II. Reynolds, Mary E. C: (1932) Regeneration in an amicronucleate infusorian. J. Exper. Zool., 62:327. Roux, J.: (1901) Faune infusorienne des eaux stagnantes des environs de Geneve. Mem. cour. l'Uni. Geneve, Geneva. Sauerbrey, Ernestine: (1928) Beobachtungen iiber einige neue

oder wenig bekannte marine Ciliaten. Arch. Protist., 62:353. Stein, F.: (1867) Der Organismus der Infusionstiere. Vol. 2. Stokes, A. C.: (1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71. Summers, F. M.: (1935) The division and reorganization of the macronuclei of Aspidisca lynceus, etc. Arch. Protist., 85:173. Turner, J. P.: (1930) Division and conjugation in Euplotes patella, etc. Univ. California Publ. Zool., 33:193. (1939) A new species of hypotrichous ciliate, Urostyla coei. Tr. Am. Micr. Soc, 58:395. von Brand, T.: (1923) Die Encystierung bei Vorticella microstoma und hypotrichen Infusorien. Arch. Protist., 47:59. Wallengren, H.: (1900) Studier ofver Ciliata infusorier. IV. Kongl. Fysio. Sail. Handl., 11:2:1. Weyer, G.: (1930) Untersuchungen liber die Morphologie und Physiologie des Formwechsel der Gastrostyla steini. Arch. Protist., 71:139. AVtchterman, R. (1942) A new ciliate from a coral of Tortugas, etc Carnegie Inst. Wash. Publ., 524:105.
:

Chapter 42

Order 3 Chonotricha Wallengren

THESE ciliates live attached to aquatic animals, especially crustaceans and have developed a peculiar organization.
as a rule, vase-form with

The body

is,

an apical peristome, around which extends a more or less complicated ectoplasmic collar or funnel and along which are found ciliary rows that lead to the deeply located cytostome and cytopharynx. The macronucleus is oval and situated centrally; there is a contractile

vacuole usually near the cytopharynx. Asexual reproduction is by lateral budding, and conjugation has been observed in a few species. Taxonomy (Kahl, 1935); distribution (Mohr, 1948).

Family Spirochonidae Stein

Genus Spirochona zone on floor of the

water.
S.

Stein.

Peristome funnel spirally wound;

ciliary

spiral furrow; attached to

Gammarus

in fresh

Many

species (Swarczewsky, 1928).

S. (Fig. 360, a).

gemmipara

80-120/* long; attached to the

gill-

plates of

Gammarus

pulex and other species. Morphology (Guilcher,

1950).

Genus Stylochona Kent. Peristomal funnel with an inner funnel. One species. S. coronata K. (Fig. 360, b). About 60/* long; on marine Gammarus.

Genus Kentrochona Rompel ( Kentrochonopsis Doflein). Peristomal funnel wide, simple, membranous; with or without a few (2)
spines.

its

K. nebaliae R. (Fig. 360, c). About 40// long; much flattened, with broad side attached by means of gelatinous substance to epiand exo-podite of Nebalia geoffroyi; salt water. Genus Trichochona Mohr. Elongate; with a long stalk; pellicle thick; a single and simple funnel; two ciliary patches, one parallel to funnel rim and the other diagonal in the deep part of funnel; one
macronucleus; one to four micronuclei; budding; marine. One species (Mohr, 1948). T. lecythoides M. (Fig. 360, d, e). Body 35-86/x by 3-28 /*; funnel
8-21. 5/i high; stalk 16-51/z long; peristomal funnel with horizontal
ciliary lines,

up

to 32; diagonal lines about 20; on the appendages of

Plate. Peristomal funnel with

the marine crustacean, Amphithoe sp.

Genus Heliochona
like spines.

numerous needle-

Taxonomy

(Wallengren, 1895; Guilcher, 1950).

847

848

PROTOZOOLOGY

Spirochona gemmipara, X300 (Hertwig); b, Stylochona c, Kentrochona nebaliae, X970 (Rompel); d, e, Trichochona lecythoides (Mohr) (d, a portion of a host's appendage with 16 attached organisms, XI 10; e, an individual, X405); f, Heliochona scheuteni, X550 (Wallengren) h, Chilodog, H. sessilis, X510 (Wallengren) chona quennerstedti, X400 (Wallengren).
Fig. 360.
a,

coronata,

X400 (Kent);

H. scheuteni (Stein)
ages of

(Fig. 360,/).

About

80-90/1 long; on append-

Gammarus

locusta; salt water.

H.

sessilis P. (Fig. 360, g).

About

60/z long;

on Gammarus

locusta;

salt water.

Genus Chilodochona Wallengren. Peristome drawn out

lips;

into

two

with a long stalk.

C. quennerstedti

W.

(Fig. 360, h).

60-1 15/* long; stalk, 40-160/x; on

Ebalia turnefacta and Portunus depurator; salt water.

References

Kahl, A.: (1935) Urtiere oder Protozoa. Darn"

Deutschlands,
etc.

Die Tierwelt

Part 30.

CHONOTRICHA
Guilcher, Yvette: (1950) Contribution a l'etude des
cilies

849

gem-

mipares, chonotriches et tentaculiferes. Univ. Paris, Thesis. S6r. A. 2369. (1951. Ann. des Sc. Nat., Zool., Ser. 11, 13:33). Mohr, J. L. (1948) Trichochona lecythroides, a new genus and species, etc. Allan Hancock Found. Publ., Occasional Papers, no.
:

5.

Swarczewsky,

B. (1928) Zur Kenntnis der Raikalprotistenfauna. Arch. Protist., 64:44. Wallengren, H.: (1895) Studier ofver ciliata infusorier. II. 77 pp.
:

Lund.

Chapter 43

Order 4 Peritricha Stein

THE region which

rior

peritrichous ciliates possess a

is

much

enlarged disk-like ante-

conspicuously ciliated.

The adoral zone

is

counter-clockwise to the cytostome viewed from the anterior end.

ciliation is more or less limited. The stalked forms produce free-swimming individuals, telotrochs. Asexual reproduction is by binary fission; and conjugation occurs commonly. The majority are free-living or attached to various aquatic animals and plants, al-

The body

though a few are

parasitic.

Taxonomy

(Kahl, 1935;

Stiller,

1939,

1940; Nenninger, 1948); structure of stalk (Precht, 1935).

Attached to submerged objects; usually no body

possesses a posterior ring of cilia

though telotroch Suborder 1 Sessilia Free-swimming; but with highly developed attaching organellae on Suborder 2 Mobilia (p. 859) aboral end
cilia,

Suborder
Without
lorica,

Sessilia

Kahl

although some with a gelatinous or mucilaginous enTribe 1 Aloricata velope Tribe 2 Loricata (p. 857) With definite pseudochitinous lorica

Tribe
end forward

Aloricata

Kahl
Family
1

Posterior end with 1-2 short spines;

swimming with peristome-bearing

Astylozoonidae

Posterior end, directly or indirectly through stalk, attached to submerged objects Anterior region a long cylindrical, highly contractile neck; contractile vacuole connected with vestibule by a long canal; reservoir of contractile vacuole distinct; with or without a thin stalk Family 2 Ophrydiidae (p. 852) Anterior portion not drawn out into a neck Family 3 Scyphidiidae (p. 852) Without stalk With stalk Family 4 Epistylidae (p. 853) Stalk non-contractile Family 5 Vorticellidae (p. 855) Stalk contractile

Family

Astylozoonidae Kahl

Genus Astylozoon Engelmann (Geleiella Stiller). Free-swimming; pyriform or conical; aboral end attenuated, with 1-2 thigmotactic stiff cilia; pellicle smooth or furrowed; wdth or without gelatinous
envelope; in fresh water.

A few species.

A.fallax E. (Fig. 361, a). 70-100m; fresh water. Genus Hastatella Erlanger. Free-swimming; body surface with 2-4 rings of long conical ectoplasmic processes; fresh water.
850

PERITRICHA
H. aesculacantha Jarocki and Jacubowska
24-40/z in stagnant water.
;

851
(Fig. 361, 6). 30-52ju

by

Genus Opisthonecta rounded; a ring of long

1.1 turns,
cilia,

Faure-Fremiet.
cilia close to

Conical;

ends

broadly

aboral end; adoral zone about

just

composed of 2 parallel rows; a papilla with about 12 long above the opening into vestibule; macronucleus sausage-

Fig. 361.
cantha,

a,

X580
d,
f,

(Jarocki);

Astylozoonfallax, X170 (Engelmann) b, Hastatella aesculapisthonecta henneguyi (c, X335 (Lynch and c, d,
;

Noble); (Kent);

Scijphidia

sessile, X65 X340 (Rosenberg)); e, X160 (Stokes); g, 0. ectatum, X160 (Mast); h, Paravorticella clymenellae, amphibiarum, X570 (Nenninger);

a cyst in

life,

Ophridium

0. vernalis,

i,

X65 (Shumway).

852

PROTOZOOLOGY

form; micronucleus; 3 contractile vacuoles connected with cyto-

pharynx; fresh water. One species.

0. henneguyi F.-F. (Fig. 361,
in
c,

d).

148-170m long; cysts about

(p.

57/z

diameter; sometimes infected by a parasitic suctorian, Endo873). Conjugation

sphaera engelmanni (Lynch and Noble, 1931)

(Rosenberg,

1940); neuromotor system

(Kofoid and Rosenberg,

1940); encystment (Rosenberg, 1938).

Family 2 Ophrydiidae Kent

Genus Ophrydium Ehrenberg (Gerda Claparede and Lachmann).

Cylindrical with a contractile neck posterior end pointed or rounded
;

variable

number
Kent

of individuals in a

common

mucilaginous mass;

pellicle usually cross-striated; fresh water.

0. sessile

(Fig. 361, e). Fully

extended body up to 300/z

long; colorless or slightly brownish; ovoid colony

up

to 5

mm. by

mm.

attached to freshwater plants.

0. vernalis (Stokes) (Fig. 361, /).

tractile; in shallow

About
/j,

250/x long; highly con-

freshwater ponds in early spring (Stokes).

(Fig. 361, g).

0. ectatum
ellae;

Mast

225-400

long; with

many

zoochlor-

colony up to 3

mm.

in diameter; in fresh

water (Mast, 1944).

Family 3 Scyphidiidae Kahl

Genus Scyphidia Dujardin. Cylindrical; posterior end attached to submerged objects or aquatic animals; body usually cross-striated;
fresh or salt water. Species (Nenninger, 1948).
S.

amphibiarum Nenninger

(Fig. 361, h).

On

tadpoles; about 76/z

long.

portion

Genus Paravorticella Kahl. Similar to Scyphidia; but posterior is much elongated and contractile; salt water, attached or
P. clymenellae

parasitic.

(Shumway)

(Fig. 361, i). 100/i long; in the colon of

the annelid, Clymenella torquata;

Woods

Hole.

Genus Glossatella Butschli. With a large adoral membrane; often attached to fish and amphibian larvae.
G. tintinnabulum (Kent) (Fig. 362, a). 30-43/x long; attached to
gills of young Triton. Genus Ellobiophrya Chatton and LwofT. Posterior end drawn out into 2 arm-like processes by means of which the organism holds fast to the gill bars of the mussel, Donax vittatus. One species. E. donacis C. and L. (Fig. 362, b). 50^ by 40/z, excluding the proc-

the epidermis and

PKRITRICHA

Fig. 362.
donacis,
d, e,

a,

Glossatella tintinnabidum

X610 (Penard);

b,

Ellobiophrya
(Stein);

X900 (Chatton and

Lwoff);

c,

Epistylis plicatilis,

X200

E. cambari (Kellicott) (d, X140; e, X340); f, E. niagarae, X150 (Bishop and Jahn); g, Rhabdostyla vernalis, X320 (Stokes); h, Opisthostyla annulata, X440 (Stokes); i, Campanella umbellaria, X180 (Schroder) j, Pyxidium vernale, X240 (Stokes) k, P. urceolatum, X 140 (Stokes) 1, Opercularia stenostoma, X140 (Udekem); m, 0. plicatilis, X40 (Stokes);
; ;

n, Operculariella parasitica,

X245 (Stammer).

Family 4 Epistylidae Kent

Genus Epistylis Ehrenberg. Inverted bell-form; individuals usually on dichotomous non-contractile stalk, forming large colonies; attached to fresh or salt water animals. Numerous species (Nenninger,
1948).

E.
often

-plicatilis

E. (Fig. 362,

c).

110-162ju long (Nenninger); colony

up

to 3

mm.

high; in fresh water.

854

PROTOZOOLOGY
d, e).

E. fugitans Kellicott. 50-60/* long; attached to Sida in early spring.

E. cambari K. (Fig. 362,

gills of

About 50 ^

long; attached to the

Cambarus.
/).
flat

E. niagarae (Fig. 362,

stomal ring prominent;

Expanded body about 16G> long; pericap makes a slight angle with the ring;

bandform macronucleus transverse to long axis, in the anterior 40-50 in a colony; attached to the antennae and body surface of crayfish (Kellicott, 1883) or to painted and snapping turtles (Bishop and Jahn, 1941). Genus Rhabdostyla Kent. Similar to Epistylis; but solitary with
third; gullet with ciliated wall;

a non-contractile stalk; attached to aquatic animals in fresh or salt

water.

Numerous

species (Nenninger, 1948).

50/x long;

R. vernalis Stokes (Fig. 362, g). About clops and Cypris in pools in early spring.

attached to Cy-

is

bent at

Genus Opisthostyla Stokes. Similar to Rhabdostyla; but stalk long, its point of attachment to submerged object, and acts like
0. annulata S. (Fig. 362, h).

a spring; fresh or salt water (Nenninger, 1948).

Body about 23^

long; fresh water.

Genus Campanella Goldfuss. Similar to

Epistylis;

but adoral

double zone turns 4-6 times; fresh water. C. umbellaria (Linnaeus) (Fig. 362, i). Colony

may

reach several

millimeters in height; individuals 130-250/* long (Kent).

Genus Pyxidium Kent. Stalk simple, not branching; peristome even when fully opened, not constricted from the body proper; frontal disk small, oblique, supported by style-like slender process arising from peristome; attached to freshwater animals and in vegetation.

Taxonomy

(Nenninger).
j).

P. vernale Stokes (Fig. 362,

long; fresh water

Solitary or few together; 70-85/z

among

algae.

P. urceolatum
plants.

S. (Fig.

362, k).

About

90/x long; fresh

water on

Genus Opercularia

Stein. Individuals similar to

Pyxidium; but

short stalk dichotomous; peristome border like a band.

O. stenostoma S. (Fig. 362, 1). When extended, up to 125/x long; attached to Asellus aquaticus and others. About 254/x long; colony 1.25O. plicatilis Stokes (Fig. 362, m).
2.5

mm. high; pond water. Genus Operculariella Stammer. Fixed

rigid;

stalk, branched, short and peristome small, without border, smooth; without disk or

frontal cilia; vestibule large (Stammer, 1948).

0. parasitica S. (Fig. 362, n). 100-1 10/u long; barrel-shaped; peri-

stome opening only 1/4 the body breadth; macronucleus about 30^

PERITRICHA
sulcatus,
tus.

855

long; parasitic in the oesophagus of Dytiscus marginalis, Acilius

Hydaticus transversalis, Graphoderes zonatus and G. bilinea-

Family 5 Vorticellidae Fromental

Genus

Vorticella Linnaeus. Inverted bell-form; colorless, yellow-

ish, or greenish; peristome more or less outwardly extended; pellicle sometimes annulated; with a contractile stalk, macronucleus band-

form; micronucleus; 1-2 contractile vacuoles; solitary; in fresh or salt water, attached to submerged objects and aquatic plants or
animals.

Numerous

species.

Taxonomy (Noland and

Finley, 1931;

*A^^

Fig. 363. a-c, Vorticella campanula (a, X400; b, part of stalk, X800; X200); d, e, V. convallaria (d, X400; e, XSOO); f-p, V. microstoma (f, g, X400; h, X840; i, telotroch, X400; j-p, telotroch-formation in vitro, X270); q, r, V. picta (q, X400; r, X800);s, t, V. monilata (s, X400; t, X800) (Noland and Finley).
c,

telotroch,

856

PROTOZOOLOGY

Kahl, 1935; Nenninger, 1948); movements of food vacuoles (Hall

and Dunihue, 1931). V. campanula Ehrenberg (Fig. 363, a-c). Usually in groups; endoplasm filled with refractile reserve granules; vestibule very large with an outer pharyngeal membrane; 50-157/* by 35-99/*; peristome 60-125/* wide; stalk 50-4150/* by 5.6-12/* fresh water. V. convallaria (L.) (Fig. 363, d, e). Resembles the last-named species; but anterior end somewhat narrow; usually without refractile granules in endoplasm; 50-95/; by 35-53/*; peristome 55-75/*
wide; stalk 25-460/* by 4-6. 5m fresh water.
;

V. microstoma Ehrenberg (Figs. 86; 363, f-p). 35-83 /* by 22-50/*; peristome 12-25/* wide; stalk 20-385/* by 1.5-4/*; common in fresh-

water infusion. Conjugation (Finley, 1943); encystment (von Brand,

1923).

V. picta (E.) (Fig. 363,

stalk 205-550/*
;

q, r).

41-63/*

by

20-37/*; peristome 35-50/*;

by

4-7/*; 2 contractile vacuoles;

with refractile gran-

ules in stalk fresh water.

(Fig. 363, s, t). Body with pellicular tuberparaglycogen (Faure-Fremiet and Thaureaux, 1944); 2 contractile vacuoles; 50-78/* by 35-57/t; peristome 36-63/* wide; stalk 50-200/* by 5-6.5/*; fresh water. Genus Carchesium Ehrenberg. Similar to Vorticella; but colonial;

V. monilata

Tatem
of

cles

composed

myonemes

in stalk not continuous, and therefore individual stalks contract independently; attached to fresh or salt water animals or plants; occasionally colonies up to 4 mm. high. Several species (Kahl,

1935; Nenninger, 1948).

Fig. 364.

a,

Carchesium polypinum, X200 (Stein);

c,

b,

C. granulatum,

X220 XI 50

(Kellicott);

Zoothamnium

arbuscula,

X200

(Stein); d, Z. adamsi,

(Stokes).

PERITRICHA
C.

857

polypinum (Linnaeus)'

(Fig. 364, a).

100-125m long; colony up

to 3

mm.

long; fresh water.

C. granulatum Kellicott (Fig. 364, b).

tractile vacuoles anterior;

About

100,u long;

2 con-

on Cambarus and aquatic plants. Genus Zoothamnium Bory. Similar to Carchesium; but myonemes (Fig. 15) of all stalks of a colony are continuous with one another, so that the entire colony contracts or expands simultaneously; fresh or salt water; colonies sometimes several millimeters high. Numerous species (Kahl, 1935; Nenninger, 1948). Development (Summers,
1938, 1938a).

Z. arbuscula Ehrenberg (Fig. 364,

c).

40-60/z long; colony

up to
cycle

more than
Z.

mm.

high; fresh water.

Morphology and
60/z long;

life

(Furssenko, 1929).

adamsi Stokes

(Fig. 364, d).

About

colony about 250/*

high; attached to Cladophora.

Tribe 2 Loricata Kahl

Peristomal margin not connected with lorica; body attached only at posterior end, and extends, out of lorica Family 1 Vaginicolidae Peristomal margin connected with inner margin of aperture of lorica; stalked disk only extends out of lorica Family 2 Lagenophryidae (p. 691)
. .

Family

Vaginicolidae

Kent

Genus Vaginicola Lamarck. Lorica without stalk, attached to substratum directly with its posterior end body elongate and cylindrical; fresh or salt water. Numerous species (Swarczewsky, 1930). V. leptosoma Stokes (Fig. 365, a). Lorica about 160/* high; when extended, about 1/3 of body protruding; on algae in pond water.
;

V. annulata S. (Fig. 365,

b).

Lorica about 120/i high; below middle,

a ring-like elevation; anterior 1/3 of body protruding, tended; pond water.

when

ex-

Genus Cothurnia Ehrenberg. Similar

(Swarczewsky, 1930).
C. canthocampti Stokes Canthocamptus minutus.

to

Vaginicola; but lorica

stands on a short stalk; fresh or salt water.

(Fig. 365, c). Lorica

Numerous
about
80/*

species

high; on

C. annulata S. (Fig. 365, d). Lorica about 55/t high; fresh water.
lorica as in Vaginicola; but complex valve-like apparatus which closes obliquely after the manner of a door when protoplasmic body conlorica with a simple or

Genus Thuricola Kent. Body and

tracts; salt or fresh water.

858

PROTOZOOLOGY

Fig. 365. a, Vaginicola leptosoma, X130 (Stokes); b, V. annulata, (Stokes); c, Cothurnia canthocampti, X150 (Stokes); d, C. annulata, X340 (Stokes); e, Thuricola folliculata, XllO (Kahl); f, Thuricolopsis kellicottiana, XllO (Stokes); g, Caulicola valvata, X760 (Stokes); h, i, Pyxicola affinis, X170 (Kent); j, P. socialis, X170 (Kent); k, Platy-

X170

cola longicollis,

(Penard); m, L. patina,

X200 (De Fromentel); X150 (Stokes);

e).

1,

Lagenophrys vaginicola, X380

n, L. labiata,

X340 (Penard).

T. folliculata (Miiller) (Fig. 365,

;

Lorica 127-170// high (Kent)

160-200/x high (Kahl) salt and fresh water.

Genus Thuricolopsis Stokes. Lorcia with an internal, narrow, adherent to lorica wall and projecting across cavity to receive and support the descended valve; protoplasmic body attached to lorica by a pedicel; on freshwater plants.
flexible valve-rest,

T. kellicottiana S. (Fig. 365,/). Lorica about 22G> long.

to Thuricola; but lorica-lid attached to aperture; fresh or brackish water. 2 species. C. valvata S. (Fig. 365, g). Lorica about 50/x high; stalk about 1/2; body protrudes about 1/3 when extended; brackish water. Genus Pyxicola Kent. Body attached posteriorly to a corneous lorica; lorica colorless to brown, erect, on a pedicel; a discoidal corneous operculum developed beneath border of peristome, which closes lorica when organism contracts; fresh or salt water. Many
species.

Genus Caulicola Stokes. Similar

P. affinis K. (Fig. 365,

water.

h, i).

Lorica about 85m long; in marsh

PERITRICHA
P. socialis (Gruber) (Fig. 365,
j).

859

Lorica about 100/t long; often in

groups; salt water.

lorica

Genus Platycola Kent. Body similar to that of Vaginicola; but always decumbent and attached throughout one side to its

fulcrum of support; fresh or salt water. Many species. P. longicollis K. (Fig. 365, k). Lorica yellow to brown when older;

about 126^ long; fresh water.

Family 2 Lagenophryidae Butschli

Genus Lagenophrys Stein. Lorica with flattened adhering surface, short neck and convex surface; "striped body" connects body with
lorica

near aperture; attached to fresh or

Lorica

salt

water animals.

Many

species (Swarczewsky, 1930). Biology (Awerinzew, 1936).

70/* by 48/*; attached to caudal minutus and Canthocamptus sp. L. patina Stokes (Fig. 365, m). Lorica 55/* by 50/*; on Gammarus. L. labiata S. (Fig. 365, n). Lorica 60/* by 55/*; on Gammarus.

L. vaginicola S. (Fig. 365,

bristles

1).

and appendages

of Cyclops

Suborder 2 Mobilia Kahl

Family Urceolariidae Stein

Genus Urceolaria Lamarck. Peristome more or

less

obliquely

placed; external ciliary ring difficult to see; horny corona of attaching disk with obliquely arranged simple teeth without radial processes;

Morphology (Wallengren, 1897). 80-140/* long; on planarians. U. paradoxa (Claparede and Lachmann) (Fig. 366, b). 70-80/*
commensal.
species.

A few

U. mitra (Siebold) (Fig. 366,

a).

in diameter; colonial forms; in the respiratory cavity of Cyclostoma

elegans.

U. karyolobia Hirshfield. 45-50/* in diameter, 20-30/* high; macronucleus lobate and conspicuous; in the mantle cavity of limpets,
Lottia gigantea

and Acmaea spp. (Hirshfield, 1949). Genus Trichodina Ehrenberg. Low barrel-shaped; with a row
cilia;

of

horny ring of attaching disk with radially arranged hooked teeth; commensal on, or parasitic in, aquatic animals. Several
posterior
species (Mueller, 1932, 1937). Structure (Wallengren, 1897a); bi-

ometry (Faure-Fremiet, 1943).

T. pediculus (Miiller) (Fig. 366,
c).

A shallow

dle of body; 50-70/* in diameter; on fish.

constriction in midThose found on Hydra and

on the

-(Fulton, 1923).

Necturus and Triturus larvae are probably this species Reproduction (Cavallini, 1931). T. urinicola Fulton (Fig. 366, d). 50-90/* long; teeth 28-36; in
gills of

860

PROTOZOOLOGY

|
J

/ft^

Fig. 366. a, Urceolaria mitra, X270 (Wallengren) b, U. paradoxa, X215 (Claparede and Lachmann); c, Trichodina pediculus, X425 (JamesClark); d, T. urinicola, X470 (Fulton); e, T. ranae (Cunha); f, T. sp., X460 (Diller); g, Cyclochaeta spongillae, X460 (Jackson); h, C. domerguei, X535 (MacLennan).
;

i,

urinary bladder of a moribund Bufo sp. (Fulton) and in frogs

Faur-Fremiet and Mugard, 1946). T. sp. Diller (Fig. 366, e). 30-4G> in diameter; on the skin and gills of frog and toad tadpoles. Division (Diller, 1928). T. ranae da Cunha (Fig. 366,/). 40-50/x in diameter, 30-5G> high; 23-31 V-shaped teeth on the attaching ring; in the urinary bladder of Rana ridibunda perezi (da Cunha, 1950). Genus Cyclochaeta Jackson. Saucer-form; peristomal surface parallel to the basal disc upper surface with numerous flat wrinkles ; basal disc composed of cuticular rings, velum, cirri, and membranel;

PERITRICHA
lae;

801

commensal on, or

parasitic in, fresh or salt water animals. Sev-

eral species.

MacLennan

(1939)

made

C. spongillae J. (Fig. 366, g).

of Spongilla fluviatilis.

About 6G>

a careful study of two species. in diameter; in interstices

C. domerguei Wallengren (Fig. 366, h, i). 23-56;u in diameter; about one-fifth high; 18-25 denticles, each with a narrow slightly curved spine; outer cuticular ring more fineby striated than inner ring; cirri longer than membranellae (MacLennan, 1939); on fresh water fishes. References

Awerinzew, G. W.:

(1936) Zur Biologie des Infusors Lagenophrys. Arch. Protist., 87:131. Bishop, E. L. Jr. and Jahn, T. L. (1941) Observations on colonial peritrichs of the Okoboji region. Proc. Iowa Acad. Sc, 48:417. Oavallini, F. (1931) La gemmazione in Trichodina pediculus. Arch. Protist., 75:167. da Cunha, A. X. (1950) Trichodina ranae, etc. Mem. Estud. Mus. Zool. Coimbra., no. 202, 11 pp. Diller, W. F.: (1928) Binary fission and endomixis in the Trichodina from tadpoles. J. Morphol. Physiol., 46:521. Faure-Fremiet, E.: (1943) Etude biometrique de quelques trichodines. Bull. Soc. Zool. France, 68:158.
: :
:

and Mugard, Helene: (1946) Une trichodine parasite en-

dovesicale chez

Rana

esculenta. Ibid., 71 :36.

:

(1944) Les globules de "paraglycogene" chez Balantidium elongatum et Vorticella monilata. Ibid., 69:3. Finley, H. E. (1943) The conjugation of Vorticella microtsoma. Tr. Am. Micr. Soc, 62:97. Fulton, J. F. Jr.: (1923) Trichodina pediculus and a new closely related species. Proc. Boston Soc. Nat. Hist., 37: 1. Furssenko, A.: (1929) Lebenscyclus and Morphologie von Zoothamnium arbuscula. Arch. Protist., 67:376. Hirshfield, H.: (1949) The morphology of Urceolaria karyolobia sp. nov., etc. J. Morphol., 85: 1. Jarocki, J. and Jakubowska, Wanda: (1927) Eine neue, solitar freischwimmende Peritriche, Hastatella aesculacantha n. sp. Zool. Anz., 73:270.* Kahl, A.: (1935) Peritricha und Chonotricha. In Dahl's Die Tierwelt Deutschlands, etc. Part 30:651. Kent, S.: (1881-1882) A manual of Infusoria. Kofoid, C. A. and Rosenberg, L. E.: (1940) The neuromotor system of Opisthonecta henneguyi. Proc. Am. Philos. Soc, 82:421. MacLennan, R. F.: (1939) The morphology and locomotor activities of Cyclochaeta domerguei. J. Morphol., 65:241. Mast, S. O. (1944) A new peritrich belonging to the genus Ophrydium. Tr. Am. Micr. Soc, 63:181. Mueller, J. F.: (1932) Trichodina renicola, a cilate parasite of the urinary tract of Esox niger. Roosevelt Wild Life Ann., 3: 139.
J.
: :

and Thaureaux,

862
(1937) 61:177.

PROTOZOOLOGY
Some
species of Trichodina, etc. Tr.

Am.

Micr. Soc.

(1948) Die Peritrichen der Umgebung von Erlangen, etc. Zool. Jahrb. Syst., 77:169. Noland, L. E. and Finley, H. E.: (1931) Studies on the taxonomy of the genus Vorticella. Tr. Am. Micr. Soc, 50:81. Penard, E.: (1922) Etude sur les infusoires d'eau douce. Geneva. Precht, H.: (1935) Die Struktur des Stieles bei den Sessilia. Arch. Protist., 85:234. Rosenberg, L. E.: (1938) Cyst stages of Opisthonecta henneguyi. Tr. Am. Micr. Soc, 57:147. (1940) Conjugation in Ophisthonecta henneguyi, etc. Proc Am. Philos. Soc, 82:437. Stammer, H.-J.: (1948) Eine neue eigenartige endoparasitische Peritriche, Operculariella parasitica n. g., n. sp. Zool. Jahrb. Syst., 77:163. Stiller, J. (1939) Die Peritrichenfauna der Nordsee bei Helgoland. Arch. Protist., 92:415. (1940) Beitrag zur Peritrichenfauna des grossen Ploner Sees in Holstein. Arch. Hydrobiol., 36:263. Stokes, A. C: (1888) A preliminary contribution toward a history of the freshwater Infusoria of the United States. J. Trenton Nat. Hist. Soc, 1:71. Summers, F. M.: (1938) Some aspects of normal development in the colonial ciliate Zoothamnium alterans. Biol. Bull., 74:117. (1938a) Form regulation in Zoothamnium alterans. Ibid., 74:

Nenninger, Ursula:

130.

Swarczewsky, B.
IV.

(1930) Zur Kenntnis der Baikalprotistenfauna. Arch. Protist., 69:455. Thompson, Sally, Kirkegaard, D. and Jahn, T. L.: (1947) Syphidia ameiuri, n. sp., etc. Tr. Am. Micr. Soc, 66:315. von Brand, T.: (1923) Die Encystierung bei Vorticella microstoma, etc. Arch. Protist., 47:59. Wallengren, H.: (1897) Studier ofver ciliata Infusorier. III. Sartryck Fysiogr. Sallsk. Handl, 8:1. (1897a) Zur Kenntnis der Gattung Trichodina. Biol. Cen:

tralbl.,

17:55.

Chapter 44
Class 2 Suctoria Claparede and
Suctoria THE Tentaculifera,

Lachmann

which have been also known as Acinetaria, do not possess any cilia or any other cellorgans of locomotion in the mature stage. The cilia are present only on young individuals which are capable of free-swimming, and lost with the development of a stalk or attaching disk, and of tentacles. Therefore, an adult suctorian is incapable of active movement. The body may be spheroidal, elliptical, or dendritic; and is covered with a pellicle and occasionally possesses a lorica. There is no cytostome, and the food-capturing is carried on exclusively by the tentacles. Tentacles are of two kinds: one is suctorial in function and bears a rounded knob on the extremity and the other is for piercing through the body of a prey and more or less sharply pointed. The tentacles may be confined to limited areas or may be distributed over the entire body surface. The food organisms are usually small ciliates and nutrition is thus holozoic. Asexual reproduction is by binary fission or by budding. The buds which are formed by either exogenous or endogenous gemmation are ciliated, and swim around actively after leaving the parent individual. Finally becoming attached to a suitable object, the buds metamorphose into adult forms. Sexual reproduction is through a complete fusion of conjugants. Relation to prostomatous ciliates (Kahl, 1931); morphogenesis (Guilcher, 1950). The Suctoria live attached to animals, plants or non-living matter submerged in fresh or salt water, although a few are parasitic.
etc.,

With only

suctorial tentacles

Body

irregular or branching
special arms;
stalk

Without proboscis or

sometimes with stolon; without Family 1 Dendrosomidae (p. 864)

With proboscis or special arms With rectractile processes bearing tentacles Family 2 Ophryodendridae With branched arms Family 3 Dendrocometidae Body more or less bilaterally symmetrical Exogenous budding and division. .Family 4 Podophryidae Endogenous budding
Pellicle thin; within or

(p. (p.

867) 867)

(p.

868)
.

without lorica; with or without stalk. Family 5 Acinetidae (p. 870) Pellicle thick; without lorica; a few tentacles, variable in form; stalk short, stout Family 6 Discophryidae (p. 875) With suctorial and prehensile tentacles; with or without lorica; exogenous budding; commensals on marine hydroids Family 7 Ephelotidae (p. 877)
.

863

864

PROTOZOOLOGY
Family
1

Dendrosomidae

Biitschli

Dendritic; often large; nucleus band-form, branched; numerous contractile vacuoles; fresh water. Taxonomy and morphology (Gonnert, 1935).

Genus Dendrosoma Ehrenberg.

Fig. 367. a, Dendrosoma radians, X35 (Kent) b, Trichophrya epistylidis (Stokes); c, T. salparum, X170 (Collin); d, T. columbiae, X200 (Wailes); e, T. micropteri, X650 (Davis); f, Erastophrya chattoni (FanreFremiet) g, Astrophrya arenaria, X65 (Awerinzew) h, Lernaeophrya capitata, X35 (P6rez); i, Dendrosomides paguri, X200 (Collin).
;

X250

SUCTORIA
tation.

865

D. radians E. (Fig. 367, a). Brownish; 1.2-2.5 mm. high; on vegeMorphology (Gonnert). Genus Trichophrya Claparede and Lachmann (Platophrya Gon-

nert).

Body

small; rounded or elongate, but variable; without stalk;

salt water.

tentacles in fascicles, not branching; simple or multiple endogenous

budding; fresh or
irregular;

T. epistylidis C.

and

L. (T. sinuosa Stokes) (Fig. 367, b).

fascicles of

Form

with

many

tentacles; nucleus

band-form,
etc., in

curved; numerous vacuoles; up to 240/x long; on Epistylis,

fresh water.
T.

Morphology (Gonnert). salparum Entz (Fig. 367, c). On various tunicates such as

Molgula manhattensis; 40-60/u long; tentacles in 2 groups; salt water; Woods Hole (Calkins). T. columbiae Wailes (Fig. 367, d). 60-75/u by 40-48/z in diameter; cylindrical; tentacles at ends; nucleus spherical; in marine plankton; Vancouver (Wailes). T. microptcri Davis (Fig. 367, e). Body elongate, irregular or rounded; up to 30-40/* long by 10-1 2n\ fully extended tentacles 1012/x long;

cytoplasm often

filled

with yellow to orange spherules; a

gill

single micronucleus; a single contractile vacuole; attached to the

of small

mouth black bass, Micropterus dolomieu. Davis (1942) states that when abundantly present, the suctorian may cause serious injury to the host.
cles; posterior

Genus Erastophrya Faure-Fremiet. Pyriform; distributed tentaend drawn out into two "arms" by means of which

the organism grasps the stalk of a peritrich; fresh water (FaureFremiet, 1943).

One

species.

E. chattoni F.-F. (Fig. 367,/).

spherical to sausage form;

Body up

to 130^ long; macronucleus

a single micronucleus; a contractile

vacuole; endogenous budding,

gemma

about 40 ju long; a commensal

on

Glossatella piscicola.

Genus Astrophrya Awerinzew.

ered

Stellate; central portion

into 8 elongate processes, each with a fascicle of tentacles;

drawn out body cov-

by sand grains and other objects. One species. A. arenaria A. (Fig. 367, g). 145-188^ in diameter; processes 80190m long; in Volga river plankton.
Genus Lernaeophrya Perez. Body
large; with

numerous short pro-

longations, bearing very long multifasciculate tentacles; nucleus

branched; brackish water. One species. L. capitata P. (Fig. 367, h). Attached to the hydrozoan, Cordylophora lacustris in brackish water; 400-500/j long; tentacles 400^
long.

Morphology (Gonnert).

866

PROTOZOOLOGY
Collin.

Genus Dendrosomides

Branched body similar

to

Dendro-

soma, but with a peduncle; reproduction by budding of vermicular form; salt water. One species. D. paguri C. (Fig. 367, i). 200-300/* long; vermicular forms 350m
long;

on the crabs, Eupagurus excavatus and E. cuanensis. Genus Rhabdophrya Chatton and Collin. Elongate, rod-form; with
;

short peduncle, not branched

tentacles distributed over entire sur-

elegans,

Rhabdophrya trimorpha, X430 (Collin); b, Staurophrya (Zacharias); c, Ophryodendron porcellanum, X220 (Collin); d, O. belgicum, X270 (Fraipont); e, Dendrocometes paradoxus, X270
Fig. 368.
a,

X200

(Wrzesnowski); f, Dendrocometides priscus, X220; g, Discosoma tenella, X220; h, Cometodendron clavatum, X220 (Swarczewsky) i, j, Podophrya
;

fixa

(i,

X400

(Wales);

j,

X220

(Collin)); k, P. elongata,

X240

(Wailes).

SUCTORIA
face;

867

macronucleus

ellipsoid;

micro nucleus small; 2-3 contractile

vacuoles; salt or brackish water. Several species.

R. trimorpha C. and C. (Fig. 368, a).

Up

to 150^ long;

on the copeinto 6

pod, Cletodes longicaudatus.

Genus Staurophrya Zacharias. Rounded body drawn out

processes.

S. elegans Z. (Fig. 368, 6). Tentacles not capitate; macronucleus round; 1-2 contractile vacuoles; about 50/z in diameter; in fresh

water.

Swarczewsky (1928) established the following genera for the forms he had found in Lake Baikal: Baikalophrya, Stylophrya, Baikalodendron and Gorgonosoma.
Family 2 Ophryodendridae Stein

Genus Ophryodendron Claparede and Lachmann. With one long

or 3-6 shorter retractile processes, bearing suctorial tentacles; on

Crustacea, Annelida, etc. salt water. Several species.

;

0. porcellanum
platycheles, etc.

Kent

(Fig. 368, c). 60-IOGVj long;

on Porcellana
form

0. belgicum Fraipont (Fig. 368, d). 38-1 14/z long; vermicular

100/i;

on Bryozoa and hydrozoans; Vancouver (Wailes).

Family 3 Dendrocometidae Stein

Genus Dendrocometes
D. paradoxus
S.

Stein.

ber of branched arms; fresh water.

(Fig. 368,

Body rounded; with variable numTaxonomy (Swarczewsky, 1928a). e). Up to 100/z long; on Gammarus
(Pestel, 1932).

pulex, G. puteanus, etc.

Morphology and biology

Stein.

Genus Stylocometes
like fresh water.
;

Arms not branched;

tentacles finger-

gills

and Lachmann). Up to HOju long; on the and on Aphrydium versatile. Genus Dendrocometides Swarczewsky. Body more or less arched; suctorial tentacles slender, pointed and simple or branched; attached to crustaceans on its broad and circular surface (SwarczewS. digitatus (Claparede

of Asellus aquaticus

sky, 1928a).

D. priscus S. (Fig. 368, /). Diameter 60-65m, height 18-20/z; on Acanthogammarus albus; Lake Baikal. Genus Discosoma S. Discoid; circular in front view; short and
pointed tentacles radially arranged, four or six in each row;
tion,

gemma-

endogenous and simple. D. tenella S. (Fig. 368, g). Diameter

victorii, etc.;

75/*,

height

10/z;

on Acantho-

gammarus

Lake Baikal.

868

PROTOZOOLOGY

Genus Cometodendron S. Body elongate; attached to substrate by a "foot," well-developed arms; short and pointed tentacles at the
ends of arms; simple endogenous gemmation.
C. clavatum S. (Fig. 368, h). 150/*

Acanthogammarus

victorii, etc.;

by 40-50/*; the Lake Baikal.

Bi'itschli

foot 20-22/*; on

Family 4 Podophryidae

Genus Podophrya Ehrenberg. Subspherical; normally with a

stalk; suctorial tentacles in fascicles or distributed

rigid

on entire body
species.

surface; encystment

common;

fresh or salt water.

Many

P. fixa Miiller (Fig. 368, i, j). Spherical; tentacles of various lengths; stalked; nucleus spheroid; one contractile vacuole; 10-28/*
long; fresh water.

P. collini Root. Ovoid; stalked; 30-60 capitate tentacles, distributed; nucleus spherical; one contractile vacuole; 40-50/t in di-

ameter; in

swamp

(Root, 1914).
k).

P. elongata Wailes (Fig. 368,

cel; tentacles distributed;

Elongate; flattened; with a pedi-

nucleus cylindrical; 95-105/* long; stalk

65-85/*

by

7-9/*;

on the marine copepod, Euchaeta japonica; Vanradiating, a few

thin; salt water.

couver.
long,

Genus Parapodophrya Kahl. Spherical; tentacles more or less conical at proximal portion; stalk
P. typha K. (Fig. 369,
a).

50-60/* in diameter; salt water (Kahl,

1931).

Genus Sphaerophrya Claparede and Lachmann. Spherical, without stalk; with or without distributed tentacles; multiplication by binary fission or exogenous budding; fresh water, free-living or parasitic.

cles

Lauterborn (Fig. 369, b). Spherical; numerous tentaabout 1/4-1/3 the body diameter; a contractile vacuole; nucleus oval; diameter about 100/z; sapropelic. S. magna Maupas. Spherical; about 50/x in diameter; numerous tentacles of different length; nucleus spheroid; standing fresh water
S. soliformis

with decaying vegetation.

S. stentoris M. Parasitic in Stentor; swarmers ciliated on posterior end; the other end with capitate tentacles; nucleus spheroid; 2 contractile vacuoles;

about

50/* long.

Genus Paracineta
;

Collin. Spherical to ellipsoidal; tentacles dis-

tributed mostly in salt water, a few in fresh water.

P. limbata (Maupas) (Fig. 369,

c,

d).

With or without gelatinous

envelope; 20-50/* in diameter; swarmer with many ciliated bands, contractile; on plants and animals in salt water.

SUCTORIA

soliformis,

X270 (Kahl); b, Sphaerophrya Paracineta limbata (c, a bud is ready to leave; d, basal part of stalk), X460 (Collin); e, Metacineta mystacina, capturing Halteria, X400 (Collin); f, Urnula epistylidis, X140 (Claparede and Lachmann); g, Lecanophrya drosera, X390 (Kahl); h, Ophryocephalus capitatum, X200 (Wailes); i, Acineta lacustris,
Fig. 369.
a,

Parapodophrya typha,
;

X200 (Lauterborn)

c,

d,

X200

(Stokes).

Genus Metacineta Biitschli. Lorica funnel-shaped, lower end drawn out for attachment; tentacles grouped at anterior end; nucleus spherical; one contractile vacuole. One species. M. mystacina (Ehrenberg) (Fig. 369, e). Lorica up to 700/x long; in fresh and salt water. Genus Urnula Claparede and Lachmann. Lorica colorless; lower end pointed, attached; aperture narrowed, round or triangular; body

870

PROTOZOOLOGY
filling lorica;

more or less

1-2 (up to 5) long active tentacles; nucleus

one or more contractile vacuoles; fresh water. U. epistylidis C. and L. (Fig. 369,/). Up to 80/x long; on Epistylis, Dendrosoma, etc. Genus LecanophryaKahl. Body rounded rectangular in cross section; anterior region bowl-shaped; somewhat rigid tentacles located on the inner surface of bowl; salt water. L. drosera K. (Fig. 369, g). 40-70m high; hollow stalk; tentacles in 3-5 indistinct rows; attached to the antennae of the copepod,
central, oval;

Nitocra typica.

Genus Ophryocephalus Wailes. Spheroidal, stalked; a single long by multiple exogenous budding from apical region; on Ephelota gemmipara and E. coronata (p. 877) salt water. One species. 0. capitatum W. (Fig. 369, h). About 55m long; tentacle up to 10G> by 1.5-5/z; Vancouver.
mobile, capitate tentacle; multiplication
;

Family 5 Acinetidae

Biitschli

Genus Acineta Ehrenberg. Lorica more or less flattened; usually with stalk; tentacles in 2 (1 or 3) fascicles; body completely or partly filling lorica; swarmer with ciliated band or completely ciliated fresh
;

or salt water.

Numerous

species (Swarczewsky, 1928a).

a).

A. tuberosa E. (Fig. 370,

Lorica 50-100m high; with stalk; salt

and brackish water.

A. cuspidata Stokes (Fig. 370, 6). Lorica cup-shaped; front end with 2 opposing sharp points; lorica 32-42^ high; on Oedogonium in
fresh water.

A. lacuslris S. (Fig. 369, i). Lorica elongate ovoid; flattened; 75185^ high; on Anacharis in pond. Genus Tokophrya Biitschli. Pyriform or pyramidal; without lorica; tentacles in

1-4 fascicles on anterior surface; stalk not rigid;

simple endogenous budding; fresh water. Several species. T. infusionum (Stein) (Fig. 370, c-e). Inverted pyramid stalk with or without attaching disk; macronucleus oval; 2 contractile vacuoles;
;

about 60m long. Relation between contractile vacuole and feeding (Rudzinska and Chambers, 1951); life span (Rudzinska, 1951). T. cyclopum (Claparede and Lachmann) (Fig. 370, /). Oval or spherical; stalk short; tentacles in 2-5 bundles; macronucleus spherical; 1-2 contractile vacuoles; about 50/x long; on Cyclops, etc. Genus Thecacineta Collin. Lorica with free margin; body usually attached to bottom of lorica, more or less long; tentacles from anterior end; salt water. Several species (Swarczewsky, 1928).

SUCTORIA

871

Fig. 370. a, Acineta tuberosa, X670 (Calkins); b, A. cuspidata, X670 (Stokes); c-e, Tokophrya infusionum (c, X400; d, a free-swimming bud; e, a young attached form, X800) (Collin); f, T. cyclopum, a young
individual,

X500

(Collin).

T. cothurnioides C. (Fig. 371, a). Lorica

about

50ju

high; stalk

knobbed; on Cletodes longicaudatus.

T. gracilis (Wailes) (Fig. 371, b). Lorica 110/x
4/jl;

by 35 M

stalk 200m

by
its

on hydrozoans.
in

Genus Periacineta Collin. Elongate lorica; attached with drawn-out posterior end; tentacles from the opposite surface
bundles; fresh water.

872

PROTOZOOLOGY
c).

P. buckei (Kent) (Fig. 371,

plate; 3 contractile vacuoles;

up

to 125ju long;

Attached end of lorica with basal on Lymnaea stagnalis

and Ranatra

linearis.

Fig. 371. a, Thecacineta colhurnioides, X400 (Collin); b, T. gracilis, (Wailes); c, Periacineta buckei, feeding on Chilodonella, X530 (Collin); d, Hallezia brachypoda, X200 (Stokes); e, Solenophrya inclusa, X230 (Stokes); f, S. per a, X230 (Stokes); g, h, Acinetopsis lentaculata

X270

(g, X130; h, X230) (Root); i, individual in Ephelota, X260;

j,

j,

Tachyblaston ephelotensis (i, a young mature form, X500) (Martin); k,

Dactylophrya roscovita, X830 (Collin).

SUCTORIA
Genus Hallezia Sand. Without
H. brachypoda (Stokes)
ing water
lorica;

873

with or without a short

stalk; tentacles in bundles; fresh water.

(Fig. 371, d). 34-42/* in diameter; in stand-

among leaves.

rectly with its

Genus Solenophrya Claparede and Lachmann. Lorica attached diunder side; body usually not filling lorica; tentacles in
about
44/x in

fascicles; fresh water.

S. inclvsa Stokes (Fig. 371, c). Lorica subspherical;

diameter; standing fresh water.

S. pera S. (Fig. 371, /). Lorica satchel-form;

about 40-45/z high;

body about 35/z long; standing fresh water. Genus Acinetopsis Robin. Lorica in close contact with body on sides; stalked; 1-6 large retractile tentacles and numerous small tentacles from apical end mainly salt water. A. tentaculata Root (Fig. 371, g, h). Lorica 187/x high; stalk 287/z long; large tentacles up to 500/z long; body about 138/z by 100/x; on Obelia commissuralis and 0. geniculata; Woods Hole (Root, 1922). Genus Tachyblaston Martin. Lorica with short stalk; tentacles distributed on anterior surface; nucleus oval; salt water. One species.
;

T. ephelotensis
;

M.

(Fig. 371, i,j). Lorica

30-93m high; stalk 20-30/x

long attached to Ephelota gemmipara.

Genus Dactylophrya Collin. Cup-like lorica, filled with the protoplasmic body; with a short stalk; 12-15 arm-like tentacles from anterior surface; salt water.

One

species.

D. roscovita C. (Fig. 371, k). About 40/t long excluding stalk; on the hydrozoan, Diphasia attenuate/,. Genus Pseudogemma Collin. Attached with a short stalk to larger
suctorians; without tentacles; endogenous budding;
ciliary

swarmer with 4

bands;

salt water.

P. pachystyla C. (Fig. 373, a). About 30/u long; stalk 3-4/z wide; swarmer 15/z by 9m; on Acineta tuberosa. Genus Endosphaera Engelmann. Spherical without lorica; without tentacles; budding endogenous; swarmer with 3 equatorial ciliary bands; parasitic in Peritricha; fresh and salt water. E. engelmanni Entz (Fig. 373, b). 15-41/x in diameter; imbedded in the host's cytoplasm; swarmer 13-19/* in diameter; in Opisthonecta henneguyi (p. 852), and other peritrichs. Genus Allantosoma Gassovsky. With neither lorica nor stalk; elongate; one or more tentacles at ends; macronucleus oval or spherical; compact micronucleus; a single contractile vacuole; cytoplasm often filled with small spheroidal bodies; development unknown; in

mammalian

intestine. Species (Hsiung, 1930).

874

PROTOZOOLOGY

ous

A. intestinalis G. (Fig. 373, c). 33-60/* by 18-37/x; attached to variciliates living in the caecum and colon of horse.

A. dicorniger Hsiung (Fig. 373,

d). 20-33/z

by

10-20ju; unattached;

in the colon of horse (Hsiung, 1928).

A. brevicorniger H. (Fig. 373, e). 23-36m by 7-1 \n; attached to various ciliates in the caecum and colon of horse.

Fig. 372. a-d,

c,

Anarma

cross-section; d, with

multiruga, Xabout 230; b, budding individual; an internal ciliated bud; e, f, Squalorophrya

g,

macrostyla,

Xabout 670; f, cross-section; Xabout 660 (Goodrich and Jahn).

Multifasciculatum elegans,

Genus Anarma Goodrich and Jahn. Radially or somewhat

laterally symmetrical;

bi-

without stalk or lorica; attached directly or by a short protoplasmic process to substratum; 1-2 fascicles of capitate tentacles; multiplication by external budding near base or by a single internal ciliated bud; conjugation; ectocommensal on Chryse-

mys
by

picta bellii (Goodrich

and Jahn, 1943).

372, a-d).

A. multiruga G. and
35-70ju;

J. (Fig.

Body
;

cylindrical, 70-150/x
folds; pellicle thin;

body surface with 7 or 8 longitudinal

cytoplasm granulated; nucleus ribbon-form 2-6 contractile vacuoles,

SUCTORIA

875

each with a permanent canal and a pore; attached directly or indirectly to the carapace and plastron of the turtle. Genus Squalorophrya Goodrich and Jahn. Elongate; radially symmetrical; lorica, rigid, close-fitting, covered with debris; with a stalk

capitate tentacles at distal end; ectocommensal on Chrysemys picta

bellii.

S. macrostyla G.

tudinal grooves;
thick,

and J. (Fig. 372, e, /). body about 90m by 40/x;

Cylindrical, with 4 longistriated stalk, short

and

about

30/* long; lorica

highly viscous with debris; nucleus

ovoid to elongate, sometimes Y-shaped; 2 contractile vacuoles, each with a permanent canal and a pore; on Chrysemys picta bellii.

Genus Multifasciculatum Goodrich and Jahn. Radially or

bilat-

erally symmetrical; stalked; without lorica; pellicle thin; several

fascicles of tentacles on distal, lateral and proximal regions of body; ectocommensal on Chrysemys picta bellii. M. elegans G. and J. (Fig. 372, g). Body ovoid; 50-90/x by 20-50/z; stalk striated, about 150-270/x long; tentacles in 4 groups; nucleus

ovoid; 1-3 contractile vacuoles; attached to the plastron of the turtle.

Family

6.

Discophryidae Collin
pedicel with

Genus Discophrya Lachmann. Elongate; a short stout

cles; contractile vacuoles,

a plate; tentacles evenly distributed on anterior surface or in fasci-

each with a canalicule leading to body

surface; mainly fresh water. Several species (Swarczewsky, 1928b).

D. elongata (Claparede and L.) (Fig. 373, /). Cylindrical; tentacles on anterior end and in 2 posterior fascicles; stalk striated; about 80ju long; on the shell of Paldina vivipara in fresh water. Genus Thaumatophrya Collin. Spherical; long stalk; tentacles distributed, tapering toward distal end; salt water. One species. T. trold (Claparede and Lachmann) (Fig. 373, g). About 75/z in
diameter.
short striated stalk;
water.

Genus Rhynchophrya Collin. Oblong; bilaterally symmetrical; a 1 main long and a few shorter tentacles; 6-10

contractile vacuoles, each with a canalicule leading to outside; fresh

One

species.

200/x long; stalk 20/z

by 50/*; by 10/z; on Hydrophilus Genus Choanophrya Hartog. Spheroidal

R. palpans C. (Fig. 373, h). 85/*

tentacles retractile, 10piceus.

tentacles; tubular, expansible at distal

particles;
ter.

to oval; stalked; 10-12 end to engulf voluminous food

macronucleus oval to spherical; a micronucleus; fresh wa-

One

species.

C. infundibulifera

H.

(Fig. 374, a). 65/t

by 60^;

fully

extended ten-

876

PROTOZOOLOGY

Fig. 373.

a,

Pseudogemma

pachystyla,

X400

(Collin);

b,

Endosphaera

engelmanni, X500 (Lynch and Noble); c, Allantosoma intestinalis, X1050 (Hsiung); d, A. dicorniger, X1300 (Hsiung); e, A. brevicorniger, X1400 (Hsiung); f, Discophrya elongata, X440 (Collin); g, Thaumatophrya trold, X1150 (Claparede and Lachmann); h, Rhynchophrya palpans, X440
(Collin).

tacles

200m long; on Cyclops ornatus. Tentacles and feeding (Farkas,

1924).

Genus Rhyncheta Zenker. Protoplasmic body attached directly to an aquatic animal with a long mobile tentacle bearing a sucker at its
;

end.

R. cyclopum Z. (Fig. 374,

b, c).

About

170/* long;

on Cyclops.

SUCTORIA

877

Fig. 374. a, Choanophrya infundibulifera, feeding on disintegrating part of a Cyclops, X400 (Collin); b, c, Rhyncheta cyclopum (b, XlOO; c, end of tentacle, X400) (Zenker); d, Ephelotagemmipara, X200 (Hertwig); e, E. coronata, X140 (Kent); f, E. plana, front view, with two attached Ophryocephalus, X35 (Wailes); g, Podocyathus diadema, X200 (Kent).

Family 7 Ephelotidae Sand

Genus Ephelota Wright. Without lorica; stalk stout, often striated; suctorial and prehensile tentacles distributed; macronucleus usually elongate, curved; on hydroids, bryozoans, algae, etc.; salt water. Numerous species. E. gemmipara Hertwig (Fig. 374, d). About 250ju by 220/x; stalk up to 1.5 mm. long; on hydroids, bryozoans, etc. E. coronata Kent (Fig. 374, e). Flattened 90-200^ long; stalk lon;

gitudinally striated (Kent)

on hydroids, bryozoans, algae,

etc.

E. plana Wailes (Fig. 374,/). 150-320/* by 100-150/z; stalk 100/*mm. long; on bryozoans; Vancouver.

878

PROTOZOOLOGY
It differs

Genus Podocyathus Kent.

spicuous lorica; salt water.
P. diadema K. (Fig. 374, hydrozoans, etc.

from Ephelota

in

having a con-

One
g).

species.

Lorica about 42^ long; on bryozoans,

References
Collin, B.: (1911) Etudes monographique sur Arch. zool. exper. gen., Ser. 5, 8:421.
(1912)11.
Ibid., 51:1.
les Acinetiens.
I.

suctorian parasite of the small mouth black Micr. Soc, 61:309. Farkas, B. (1924) Beitrage zur Kenntnis der Suctorien. Arch. Protist., 48:125. Faure-Fremiet, E.: (1943) Commensalisme et adaption chez un acinetien: Erastophrya chattoni, etc. Bull. soc. zool. Fr., 68:145. Gonnert, R. (1935) Ueber Systematik, Morphologie, Entwicklungsgeschichte und Parasiten einiger Dendrosomidae, etc. Arch. Protist., 86:113. Goodrich, J. P. and Jahn, T. L.: (1943) Epizoic Suctoria from turtles. Tr. Am. Micr. Soc, 62:245. Gtjilcher, Yvette: (1950) Contribution a l'etude des cilies gemmipares, chonotriches et tentaculiferes. Uni. Paris Thesis, Ser. A. 2369 (1951 Ann. des Sc. Nat., Zool., Ser. 11, 13:33). Hsiitng, T. S.: (T928) Suctoria of the large intestine of the horse. Iowa State College J. Sc, 3:101. (1930) A monograph on the Protozoa of the large intestine Ibid., 4:350. of the horse. Kahl, A.: (1931) Ueber die verwandtschaftlichen Beziehungen der Suctorien zu den Prostomen Infusorien. Arch. Protist., 73:424. (1934) Suctoria. Grimpe's Die Tierwelt der Nord- und Ostsee. Part 26. Leipzig. Kent, S. (1881-1882) A manual of the Infusoria. Pestel, B.: (1932) Beitrage zur Morphologie und Biologie des Dendrocomctes paradoxus. Arch. Protist., 75:403. Root, F. M.: (1914) Reproduction and reactions to food in the suctorian, Podophrya collini n. sp. Ibid., 35:164. (1922) A new suctorian from Woods Hole. Tr. Am. Micr. Soc, 41:77. Rudzinska, Maria A.: (1951) The effect of overfeeding and starvation on the life span and reproduction of Tokophrya infusionum, etc J. Gerontol., 6, Suppl. 3:144. and Chambers, R.: (1951) The activity of the contractile vacuole in a suctorian (Tokophrya infusionum). Biol. Bull., 100:

Davis, H.

S.: (1942)

bass, etc. Tr.

:

Am.

I.

49.

Swarczewsky,

B.: (1928) Zur Kenntnis der Baikalprotistenfauna. Arch. Protist., 61:349. Ibid., 62:41. (1928a) II. (1928b) III. Ibid., 63:1. Ibid., 63:362. (1928c) IV. Wailes, G. H.: (1928) Dinoflagellates and Protozoa from British Columbia. Vancouver Museum Notes, 3:25.

Chapter 45
Collection, Cultivation,

and Observation

of

Protozoa

Collection

N THE

foregoing chapters

species of Protozoa

it has been pointed out that various have characteristic habitats and that many

of free-living forms are widely distributed in bodies of water: fresh,

brackish, and salt; while the parasitic forms are confined to specific

host animals. Of free-living Protozoa

large

many

species

may

occur in

numbers within a small area under favorable conditions, but

the majority are present in comparatively small numbers. If one

who

has become acquainted with the representative forms, intends to make collection, it is well to carry a compound microscope in order to avoid bringing back numerous jars containing much water, but

few organisms. Submerged plants, decaying leaves, surface scum, ooze, etc., should be examined under the microscope. When desired forms are found, they should be collected together with a quantity of water in which they occur. When the material is brought into the laboratory, it is often necessary to concentrate the organisms in a relatively small volume of water. For this purpose the water may partly be filtered rapidly through a fine milling cloth and the residue quickly poured back into a suitable container before filtration is completed. The container should be placed in a cool moderately lighted room to allow the organisms to become established in the new environment. Stigmabearing Phytomastigina will then be collected in a few hours on the
side of the container, facing the strongest light,

and the members

of

be found among the debris on the bottom. Many forms will not only livejong, but also multiply in such a container. For obtaining large freshwater amoebae, fill several finger bowls with the collected material and water, and place one or two rice grains to each. After a few days, examine the bottom surface of the bowls under a binocular dissecting microscope. If amoebae were included in the collection, they will be found particularly around the rice grains. Pipette them off and begin separate cultures (p. 881). In order to collect parasitic Protozoa, one must, of course, find the host organisms that harbor them. Various species of tadpoles, frogs, cockroaches, termites, etc., which are of common occurrence or easily obtained and which are hosts to numerous species of Protozoa, are useful material for class work.
Sarcodina
will

879

880
Intestinal Protozoa of

PROTOZOOLOGY
man
are usually studied in the faeces of an
collected.

infected person. Natural

movement should be

Do

not use

oily purgatives in obtaining faecal specimens, as

they

make the

droplets.

by the presence of numerous oil must be thoroughly cleaned and dry, and provided with a cover. Urine or water must be excluded completely. The faeces must be examined as soon as possible, since the active
microscopical examination difficult

The

receptacle

trophozoites degenerate quickly once leaving the

If

human

intestine.

must not be older than one hour or two. In case this is not possible, wrap the container with woolen cloth while transporting, the organisms may live for several hours. Care must however be exercised during the microscopical examination, as there will be present unavoidably a large number of degenerating forms. If the stool is formed and normal, it would contain usually encysted forms and no trophozoites if the host is infected by a protozoan, unless mucus, puss, or blood is present in it. Examination of such faeces can be delayed, as the cysts
dysenteric or diarrhoeic stools are to be examined, they
are quite resistant (p. 450).

Cultivation

For extensive study or for class work, a large number of certain species of Protozoa are frequently needed. Detection and diagnosis of human Protozoa are often more satisfactorily made by culture method than by microscopical examination of the collected material. Success in culturing Protozoa depends upon several factors. First an abundant supply of proper food material must be made available. For example, several species of Paramecium live almost exclusively on bacterial organisms, while Didinium and allied ciliates depend upon Paramecium and other ciliates as sources of food supply. For cultivating chromatophore-bearing forms successfully, good light and proper kinds and amount of inorganic substances are necessary. In the second place, the temperature and chemical constituents of
the culture
rule,

medium must be adjusted to suit individual species. As a lower temperatures seem to be much more favorable for culture than higher temperatures, although this is naturally not the case with those parasitic in homoiothermal animals. Furthermore, proper
hydrogen ion concentration of the culture must be maintained. In the third place, both Protozoa and Metazoa which prey upon the forms under cultivation must be excluded from the culture. For instance, it is necessary to remove Didinium nasutum in order to obtain a rich culture of Paramecium. For successful culture of Amoeba proteus, Aeolosoma, Daphnia, Cyclops, etc., must be excluded from
the culture.

COLLECTION, CULTIVATION, OBSERVATION

881

Mixed cultures of many free-living Protozoa are easily maintained by adding from time to time a small amount of ripe hay-infusion or dried lettuce powder to the collected water mentioned before. Chilomonas, Peranema, Bodo, Arcella, Amoeba, Paramecium, Colpoda, Stylonychia, Euplotes, etc., often multiply in such cultures. To obtain a large number of a single species, individuals are taken out under a binocular dissecting microscope by means of a finely drawnout pipette and transferred to a suitable culture medium. Such a
culture
is

called a

mass or

stock culture. If

a culture

is

started with a
clone or a

single individual, the resulting population

makes up a

pure line

Aside from the cultures of blood-inhabiting Protozoa and of some

100 free-living forms, the protozoan cultures are by no means "pure"
cultures in the bacteriological sense, even
if

only one species of Proin-

tozoa

is

present, since bacteria

and other microorganisms are

variably abundantly present in them.

A. Free-living Protozoa

To

deal with

all

the culture media employed by numerous workers

Protozoa is beyond the scope of the present work. Here only a few examples will be given. For further information, the reader is referred to Belaf (1928), Needham et al. (1937),
for various free-living
etc.

Chromatophore-bearing
fluids.

flagellates.

There are a number of culture

Two examples:
Peptone or tryptone

(a)

(b)

882
factory one
distilled

PROTOZOOLOGY

is as follows: Fill a finger bowl with about 150 cc. of glass water and place 4 rice grains on the bottom. Let the dish stand for a few days, and then introduce with a pipette a number of desired flagellates from a mass culture into it. Cover the bowl and keep it at about 20 C. Mast (1939) used the following media for Chilomonas Paramecium. (a) Glucose-peptone solution:

Peptone Glucose

8 gm.

2 gm.

Water
(b)

1000
solution:

cc.

Acetate-ammonium

COLLECTION, CULTIVATION, OBSERVATION

Ca 3 (P0 4 ) 2
Pyrex water
0.002 gm. 1000 cc.

883

Pelomyxa
with 150

carolinensis.

These amoebae grow well in a finger bowl

cc. of redistilled

cium are added

daily.

water to which large numbers of ParamePace and Belda (1944) advocate the following

solution instead of distilled water:

K2HPO4

KH P0
2

Mg

CaCl 2 3 (P0 4 ) 2 4H 2

Pyrex water

0.08 0.08 0.104 002 1000

.

gm. gm. gm. gm.

cc.

Small mono- or di-phasic amoebae. Musgrave and Clegg's medium, modified by Walker, is as follows:

Agar

NaCl
Liebig's beef -extract

2.5 gm. 0.05 gm. 0.05 gm.

2
cc.

Normal

NaOH

Distilled water

100

cc.

and other Testacea. The testaceans commonly multiply mixed culture for several weeks after the collection was made. Hegner's method for Arcella: Pond water with weeds is shaken up violently and filtered through eight thicknesses of cheese cloth, which
Arcella
in a

prevents the passage of coarse particles.

The

filtrate is distributed

among Petri dishes, and when suspended

also for Difflugia

particles

have settled down

is

to the bottom, specimens of Arcella are introduced. This will serve

and other testaceans.

Hay

or rice infusion

also

a good culture

medium

for these organisms.

Actinophrys and Actinosphaerium. Belaf cultivated these heliozoans successfully in Knop's solution:

Magnesium sulphate
Calcium nitrate Potassium phosphate Potassium chloride
Iron chloride
Distilled

25 gm.
1

gm.

25 gm.

0.12 gm.
trace

water

1000

cc.

Freshwater dilates.

They are easily cultivated

left

in a

weak

infusion

of hay, bread, cracker, lettuce leaf, etc.

The battery

jars containing

the infusions should be

ow

a rich bacterial

growth

standing uncovered for a few days to alin them. Seed them with material such

..

884
as

PROTOZOOLOGY

sired, culture

submerged leaves or surface scum containing the ciliates. If demay be started with a single individual in a watch glass. Collection, cultivation and sterilization of Paramecium (WichPure culture

terman, 1949).

free-living flagellates and certain ciliates have in recent years been successfully cultured free from any other associated organisms. The protozoan to be cultivated must be freed from other
this, washing, dilution, migration and have been used. For information, the reader is referred to Glaser and Coria (1930), Claff (1940), Taylor and Van Wagentock (1941), Kidder (1941), etc. Free-living Phytomastigina. Many media are known. See Pringsheim (1926, 1937, 1946), Hall (1937, 1941), Hutner and Provasoli

Many

Protozoa and bacteria. For

bactericidal agents

(1951), etc.

basal

Tetrahymena and allied forms. medium as quoted below:

Kidder, Dewey and

Thiamine HC1
Biotin (free acid) Choline CI

Parks use a

y per ml
DL-alanine L-arginine
L-aspartic acid

7 per ml
1.00

110

206
122 10

0.0005 1.00
100 25

Glycine L-glutamic acid

L-histidine

DL-isoleucine
L-leucine
L-lysine

DL-methionine L-phenylalanine
L-proline

DL-serine

DL-threonine L-tryptophane DL-valine

233 87 276 344 272 248 160 250 394 326 72 162

MgSo -7H 0. Fe(NH (S0 MnCl -4H 0.

4
2 4) 2

4) 2
.

6H

ZnCl 2 CaCl 2 -2H 2 0...

0.5 0.05 50
5

CuCl 2 -2H 2 0...

FeCL-6H 0.
2

..

K HP0
2

4 4

KH OP
2

1.25 1,000 1,000 30 20 25

10

Guanylic acid Adenylic acid.

Cytidylic acid Uracil

Ca pantothenate
Nicotinamide Pyridoxine HC1
Pyridoxal

HC1

0.10 0.10 1.00 0.10

0. 10

Dextrose

Na

acetate

Pyridoxamine HC1
Riboflavin Pteroylglutamic acid

Tween85
Protogen

2,500 1,000 700

1

0.10 0.01

unit

B. Parasitic Protozoa

man. There are numerous media which have been used successfully by several investigators.
Intestinal flagellates of

COLLECTION, CULTIVATION, OBSERVATION

885

(a) Ovo-mucoid medium (Hogue, 1921). White of two eggs are NaCl solubroken in a sterile flask with beads. Add 200 cc. of 0.7 tion and cook the whole for 30 minutes over a boiling water bath, shaking the mixture constantly. Filter through a coarse cheese cloth and through cotton-wool with the aid of a suction pump. Put 6 cc. of the filtrate in each test tube. Autoclave the tubes for 20 minutes under 15 pounds pressure. After cooling, a small amount of fresh faecal

material containing the flagellates

is

introduced into the tubes. Incu-

bate at 37C.
of 100 cc. of sterile

serum water (Hogue, 1922). Composed cc. of sterile sheep serum water (dilution 1:3). 15 cc. to each tube. Trichomonas hominis, T. tenax, and Retortamonas intestinalis grow well. Trichomonas vaginalis. Johnson and Trussell (1943) reported the following mixture the most suitable medium
(b)

Sodium

chloride sheep

0.95% NaCl and 10-15

Bacto-peptone

886

PROTOZOOLOGY
For Trichomonas termopsidis, a small amount
of Loeffler's

In solution A, Trichomonas sp. and Tricercomitus termopsidis were

cultivated.

blood serum and cellulose were added. All three flagellates were cultured for over three years. In solution U to which 0.01 per cent blood

serum, cellulose and charcoal, were added, Trichonympha sphaerica (from Termopsis angusticollis) grew well and multiplied up to two
so. The was inoculated with the entire hindgut of a termite and kept at room temperature. Lophomonas blattarum and L. striata. A mixture of one sterile egg-white and 100 cc. of sterile Ringer's solution, to which a small amount of yeast cake is added, is an excellent culture medium. Incubation at room temperature; subcultures every 4-6 days. Trypanosoma and Leishmania. Novy, MacNeal and Nicolle (NNN) medium: 14 gm. of agar and 6 gm. of NaCl are dissolved by

weeks, although T. campanula and T. collaris failed to do

culture in a test tube

cc. of distilled water. When the mixture cools to about 50C, 50-100 cc. of sterile defibrinated rabbit blood is gently added and carefully mixed so as to prevent the formation of bubbles. The

heating in 900

blood agar
of

is

now

distributed

among

sterile test

tubes to the height

about 3 cm., and the tubes are left slanted until the medium becomes solid. The tubes are then incubated at 37C. for 24 hours to determine sterility and further to hasten the formation of condensation water (pH 7.6). Sterile blood or splenic puncture containing Trypanosoma cruzi or Leishmania is introduced by a sterile pipette to the condensation water in which organisms multiply. Incubation at 37C. for trypanosomes and at 20-24C. for Leishmania. For cultivating T. gambiense and T. rhodesiense, Tobie, von Brand and Mehlman (1950) used the following medium: (a) Base. 1.5 gm. Bacto-beef, 2.5 gm. Bacto-peptone, 4 gm. sodium chloride and 7.5 gm. Bacto-agar, are dissolved in 500 cc. distilled water. After adjusting pH to 7.2-7.4 with NaOH, autoclave at 15 lbs pressure for 20 minutes. Cool this to about 45C, then add whole rabbit blood which had been inactivated at 56C. for 30 minutes, in
the proportion of 25
cc.

blood to 75

cc. base,

using 0.5 per cent sterile

sodium

citrate to prevent the coagulation.

test tubes (5 cc.

This base is placed in each and slanted) or in flasks (25 cc), and allowed

to solidify.
(b)

amounts

Liquid phase. Sterile Locke's solution. This is added in of 2 cc. (to test tubes) or 10-15 cc. (to flasks), and cotton

plugs are applied. The trypanosomes are said to grow well and to reach the peak population in 10-14 days.

Entamoeba

barreti.

Barret and Smith

(1924) used a mixture of

COLLECTION, CULTIVATION, OBSERVATION

9 parts of

887

0.5% NaCl and

part of

human

blood serum. Incubation

at 10-15C.

gastric

and Geiman (1938) used a mixture of "ground alum" salt 0.5 gm., and distilled water 100 cc. About 2 mg. of sterile rice starch is added to each culture tube at the time of inoculation. Culture at 20-30 C. and subE. invadens.

Ratcliffe
0.3 gm.,

mucin

culture every 7 days.

E. histolytica and other amoebae of man.

ture was

The

first

successful cul-

made by Boeck and Drbohlav

(1925)

who used the

follow-

ing media.
(a) Locke-egg-serum (LES) medium. The contents of 4 eggs (washed and dipped in alcohol) are mixed with, and broken in, 50 cc. of Locke's solution in a sterile flask with beads. The solution is made

up

as follows:

NaCl
CaCl 2

KC1
NaHCC-3
Glucose
Distilled

9 gm. 0.2 gm. 0.4 gm. 0.2 gm.

2 5 gm.
.

water
so that

1000

cc.

The emulsion
is

is

now tubed

when coagulated by

heat, there

1-1.5 inches of slant. These tubes are

70C.
for

now slanted and heated at until the medium becomes solidified. They are then autoclaved

20 minutes at 15 pounds pressure (temperature must be raised and lowered slowly). After cooling the slant is covered with a mixture of 8 parts of sterile Locke's solution and 1 part of sterile inblood serum. The tubes are next incubated to The culture tubes are inoculated with a small amount of faecal matter containing active trophozoites. Incubation at 37C. Yorke and Adams (1926) obtained rich cultures by inoculating this medium with washed and concentrated cysts of E. hisactivated

human

determine

sterility.

tolytica in

24 hours. Locke-egg-albumin (LEA) medium. The serum in LES medium is replaced by 1% solution of crystallized egg albumin in Locke's solution which has been sterilized by passage through a Berkefeld
(b)
filter.

Dobell and Laidlaw (1926) used Ringer's solution instead of

Locke's.
(c) Ringer-egg-serum (RES) or Ringer-egg-albumin (REA) medium. Solid medium is the same as that of (a) or (b), but made up in Ringer's solution which is composed of

888

PROTOZOOLOGY
NaCl

KC1
CaCl 2
Distilled

water

9 gm. 0.2 gm. 0.2 gm. 1000 cc.

latter
is

The covering liquid is serum-Ringer or egg-albumin. The prepared by breaking one egg white in 250 cc. of Ringer's
which
is

solution

passed through a Seitz

filter.

bae, a small
for 1 hour)
(d)

amount of

sterile solid rice-starch

Before inoculating with amoe(dry-heated at 180C.

is added to the culture tube. Horse-serum-serum (HSS) or Horse-serum-egg-albumin (HSA) medium. Whole horse-serum, sterilized by filtration, is tubed and slanted at 80C. for about 60-70 minutes (do not heat longer). When the slants have cooled, they are covered with diluted serum or egg-albumin given for (c). The tubes are incubated for sterility and sterile rice-starch is added immediately before inoculation. Frye and

Meleny (1939) substituted the liquid portion of this medium by 0.5% solution of Lily liver extract No. 343 in 0.85% NaCl.
(e)

Liver-agar-serum (LAS)

(1930) used the following

medium. Cleveland and Sanders medium:

30 gm. 1000 cc.

Liver infusion agar

(Difco dehydrated)

Glass distilled water

The medium
solution.
rice is

is

tubed, autoclaved, and slanted.

The

slants are cov-

ered with a 1:6 dilution of sterile fresh horse serum in

0.85% NaCl

mm.

loop of sterile rice flour or powdered unpolished

of the rice flour debris

making subculture, remove 2 or 3 drops from the bottom with a sterile pipette. (/) Egg-yolk-saline medium (Balamuth and Sandza, 1944). Two eggs are hard-boiled. Upon cooling, the egg white is discarded and the yolks are crumbled in a beaker containing 125 ml of 0.8 per cent sodium chloride solution. The mixture is boiled for 10 minutes, and
added
to each tube. In after replacement of evaporated water the infusion
is

filtered

by

suction

pump and

restored to 125 ml.

The

filtrate is

autoclaved 20
after

minutes at 15 pounds pressure. Upon cooling, a

of yolk settles,

slight precipitation

and

is

removed by simple

filtration,

which

125 ml of
total salt

N/15 phosphate buffer (pH 7.5) is added, making the concentration N/30 phosphate solution in 0.4 per cent
is

sodium

chloride. This final mixture

is

tubed in 5 ml amounts, autosterile rice starch is

claved as before, and then

stored under refrigeration until use.

Before introducing amoebae a loop of

added to

each tube.

COLLECTION, CULTIVATION, OBSERVATION

To
inhibit bacterial

889

growth in cultures of Entamoeba, various have been tried. For example, Spingarn and Edelman (1947) found that when streptomycin was added in the amount of 1000-3000 units per cc. to culture of E. histolytica, the survival of the amoebae in culture was prolonged from an average of 8 days to 33.7 days, which effect was apparently due to the inhibition of bacteria. Encystment of Entamoeba histolytica is usually brought about by first cultivating the organisms in starch-free media and then by transferring them into media with starch. Balamuth (1951) recommends a diphasic medium of the following composition: 2 gm. of Wilson liver concentrate powder is brought to boiling in 80 ml. distilled water and filtered. Then 6.4 ml. of 0.25 molar Na P0 4 12 H 2 and 7.6 ml. of 1.0 molar potassium phosphate buffer (in the ratio of 4.7 parts K 2 HP0 4 to 0.3 part KH 2 P0 4 ) are added. By adding distilled water in a volumetric flask bring the mixture to 100 ml. Transfer it to a beaker and add 3 gm. Bacto-agar. Heat gently until agar dissolves; then autoclave for 20 minutes at 15 lbs pressure. The pH should be about 7.2. The overlay is prepared by mixing doublestrength eggyolk and normal horse serum (10:1) and rice starch is added last. Plasmodium. Bass and John's (1912) culture is as follows: 10 cc. of defibrinated human blood containing Plasmodium and 0.1 cc. of 50% sterile dextrose solution are mixed in test tubes and incubated at 37-39C. In the culture, the organisms develop in the upper layer of erythrocytes. Since that time a number of investigators have undertaken cultivation of different species of Plasmodium. For information the reader is referred to Geiman, Anfinsen et al. (1946) and Trager (1950). Balantidium coli. Barret and Yarbrough (1921) first cultivated this ciliate in a medium consisting of 16 parts of 0.5% NaCl and 1
antibiotics
3
.

part of inactivated

blood serum. The medium is tubed. of the faecal matter containing the trophozoites is made into the bottom of the tubes. Incubation at 37C. Maximum development is reached in 48-72 hours. Subcultures are made every second day. Rees used a mixture of 16 parts of Ringer's solution and 1 part of Loeffler's derrydrated blood serum. Atchley (1935) employed a medium composed of 4 parts of Ringer's solution and 1 part of faeces, which is filtered after 24 hours, centrifuged and sterilized by passage through a Seitz filter. Nelson (1940) also used 1 part of caecal contents of pig in 9 parts of Ringer's solution, which mixture is passed through a sieve and then filtered through a thick absorbent cotton. Balantidium which shows posiInoculation of a small

human

amount

890
tive geotropism,

PROTOZOOLOGY

is freed of faecal debris by passage downward through cotton in V-tube. The ciliates are introduced into the culture tubes. Incubation at 37C. Subcultures are made every 7-22 days. Nelson found that autoclaved medium is unsuitable until a living bacterial population has been established. Balantidium can also be cultivated in the media given for the intestinal amoebae.

Microscopical examination

Protozoa should be studied as far as possible in

preparations while indispensable in revealing
structures, cannot replace fresh preparations.
of standard size, 3"
thin.

life.

Permanent
slides

many

intracellular

The microscopic

by

I",

should be of white glass and preferably

The so-called No. 1 slides measure about 0.75 mm. in thickness. For darkfield illumination thin slides are essential. No. 1 coverglasses should be used for both fresh and permanent preparations. They are about 130-1 70/x thick. The most convenient size of the coverglass is about 7/8 square inch which many prefer to circular ones. The slides and coverglasses must be thoroughly cleaned before
being used. Immerse them in concentrated mineral acids (nitric acid is best fitted) for 10 minutes. Pour off the acid, wash the slides and coverglasses for about 10 minutes in running water, rinse in distilled
water, and keep them in 95% alcohol. When needed they are dried one by one with clean cheese cloth. Handle slides and covers with a pair of forceps. If thumb and fingers are used, hold them edgewise.

A. Fresh preparations

ercised to avoid pressure of the coverglass

In making fresh preparations with large Protozoa care must be exon the organisms as this

will cause deformities. If small bits of detritus or debris are included

in the preparation, the coverglass will

organisms

be supported by them and the not be subjected to any pressure. Although ordinary slides are used most frequently, it is sometimes advisable to use a depression slide especially for prolonged observation. To make a preparation with this slide, a small drop of water containing specimens is placed in the center of a coverglass, and is covered by a small
will
1 cm. in diameter), which in turn is covwith a thin coat of vaseline along the edge of the depression, so as to make an air-tight compartment. In turning over the whole, care must be taken to prevent the smaller circular cover from touching any part of the slide, as this would cause the water to run down into the depression. Nemeczek (1926) seems to

circular coverglass (about

ered

by a depression

slide

have been the

first

one who used the second coverglass for this prepa-

COLLECTION, CULTIVATION, OBSERVATION

891

ration. If the Protozoa to be examined are large and observation can be made under a low power objective, the small coverglass should be omitted. As far as possible examine fresh preparations with low power objectives. The lower the magnification, the brighter and the larger the field. The microscopical objects can quickly and easily be measured, if an ocular micrometer division has been calculated in combination with different objectives. The free-living ciliates swim about so actively as to make their observation difficult. However, an actively swimming ciliate will sooner or later come to stop upon coming in contact with various debris, air bubbles or margin of the coverglass to allow a study of its structure. Various reagents recommended for retardation of swimming movements of ciliates, bring about deformities in the organisms and therefore, must not be used; but a drop of saturated solution of methyl cellulose may be added to a ciliate preparation to retard the active movement of the organism without causing any visible abnormality (Marsland, 1943).

For observation of

cilia, flagella,

extruded polar filament of Microit

sporidia, etc., the so-called changeable condenser is useful, since

gives both bright and dark fields under dry objectives.

The ordinary

dark field condenser is used almost exclusively in conjunction with an oil immersion objective and therefore for very active organisms a great deal of time is often lost before satisfactory observation is made. The phase microscope is highly useful in studying various
intracellular structures in
life.

When

treated with highly diluted solutions of certain dyes, living

Protozoa exhibit some of their organellae or inclusions stained without apparent injury to the organisms. These vital stains are usually prepared in absolute alcohol solutions. A small amount is uniformly applied to the slide and allowed to dry, before water containing Protozoa is placed on it. Congo red (1 1,000) is used as an indicator, as its red color of the salt changes blue in weak acids. Janus Green B (1:10,000-20,000) stains chondriosomes. Methylene blue (1:10,000 or more) stains cytoplasmic granules, nucleus, cytoplasmic processes, etc., Neutral red (1:3,000-30,000) is an indicator: yellowish red (alkaline), cherry red (weak acid), and blue (strong acid). It also stains nucleus slightly. Golgi bodies are studied in it, though its specific^ for this structure is not clear. Parasitic Protozoa should be studied in the tissue or body fluids in which they occur. When they are too small in amount to make a suitable preparation, one of the following solutions may be used.
:

892

PROTOZOOLOGY
NaCl
for

Physiological salt solution. Widely used concentrations of

solutions are 0.5-0.7% for cold-blooded animals

and 0.8-0.9%

warm-blooded animals.
Ringer's solution.

ready

(p. 887).

The one Dobell advocated has been given Another frequently used solution consists of
0.8 0.02 0.02 0.02 100

al-

NaCl KC1
CaCl 2

gm. gm. gm.

gm.)
cc.

(NaHC0 3
Glass distilled water

For demonstrating organellae, the following reagents which kill upon application, may be used on living Protozoa. LugoFs solution. This is made up of potassium iodide 1.5 gm., water 25 cc, and iodine 1 gm. The solution deteriorates easily. Flagella and cilia stain clearly. Glycogen bodies stain ordinarily reddish brown. Cysts of intestinal Protozoa are more easily studied in
the Protozoa
Lugol's solution.

Sudan

III

and IV.

2% absolute alcohol solution diluted before use

45% alcohol.
solution in

with the same amount of

Methyl green.
Nigrosin.

1%

1%

acetic acid solution

Neutral fats are stained red. makes an

excellent nuclear stain.

used in smears and air-dried makes the and ciliates stand out clearly. In the case of faecal examination if the stool is dysenteric, a small portion is placed by a tooth-pick or platinum loop on a slide and
solution
if

10%

pellicular patterns of flagellates

covered with a cover

cles

glass.

Before placing the cover,

all

large parti-

must be removed quickly so that the smear will be uniformly thin. Smears of diarrhoeic stools can be made in a similar way. But
formed or semiformed, a small drop of warm is first placed on the slide, and a small portion of the faeces, particularly mucus, pus or blood, is emulsified in it. The whole is covered by a coverglass. The faecal smear should not be too thick or too thin for a satisfactory observation. If the smear is too thick, it will be impossible to distinguish objects clearly, and on the other hand, if it is too thin, there will be much
if

the faecal material

is

(37C.)

0.85% NaCl

solution

thickness of the smear

time lost in observing widely scattered Protozoa. The optimum is one through which the print of this page

can be read.

The success in faecal examination for intestinal Protozoa depends almost entirely on continued practice, since the faecal matter contains myriads of objects which may resemble Protozoa (Fig. 375,

COLLECTION, CULTIVATION, OBSERVATION

c-h). Aside

S93

from certain coprozoic Protozoa

organism which
is

(p.

24) which appear in

all

old faeces, Blastocystis hominis (Fig. 375, c-f) occur in almost

faeces. This
is

considered to be a fungus and harma narrow peripheral

less to its host,

usually spherical and measures about 5-25ju in

is

diameter. Within a very thin membrane, there

1

or 2 nuclei and several refractile grancytoplasmic layer in which ules are present. The cytoplasmic ring encloses a large homogeneous

body which
ler.

is

the cytoplasm

may

somewhat eosinophile, but not be more abundant and the

iodinophile. In

inclusion

some body smal-

Dividing forms appear peanut-shaped. Blastocystis (Grasse,

1926; Reyer, 1939).

Fig. 375.
cystis

a,

Sphaerita in a stained trophozoite of Entamoeba

coli; b,

Nucleophaga
hominis

in a stained trophozoite of
(in
;

Iodamoeba
,

butschlii;

c, d,

Blasto-

an unstained smear) e, f stained Blastocystis hominis; g, an epithelial cell from a faecal smear; h, a polymorphonuclear leucocyte with three ingested erythrocytes. All X1150 (Kudo).

In a

number

of parasitic Protozoa, there occur foreign organ-

isms which

may

be mistaken for food inclusions or chromatin.

They

named by Dangeard and Nucleophaga (Fig. 375, a, b). The former occurs in the cytoplasm and the latter in the nucleus of the host protozoan. These parasites are spherical and about 0.5-lju in diameter; they are found most frequently in spherical masses composed of varying numbers of individuals. Nucleophaga appears to destroy the
are vegetable organisms which were
as Sphaerita

host nucleus. Degenerating epithelial

h)

cells

or leucocytes (Fig. 375,

g,

simulate parasitic amoebae. Fishes and birds are often infected by Coccidia and when they are consumed as food, the oocysts
pass the alimentary canal unchanged and appear in the stools.

may

Sphaerita (Chatton and Brodsky, 1909; Mattes, 1924; Becker, 1926;

894

PROTOZOOLOGY

Sassuchin, 1928; Sassuchin et al., 1930; Jahn, 1933; Kirby, 1941). The cysts of intestinal Protozoa are, as a rule, distributed through-

out the formed faeces and difficult to detect in small portions of the voided specimens. Flecks of mucus in the fluid stool obtained by use of a saline purge may contain more numerous cysts than naturally
passed one. Several methods for concentrating cysts for microscopical examination are known. The simplest one is to emulsify thoroughly a small mass of faeces about the size of a lump sugar in a dish by adding a small amount of once-boiled tap water. Add to it about 500 cc. of water and pour the whole emulsion into a glass cylinder, and let it stand for about 15 minutes. Remove the scum floating on the surface and draw off the turbid fluid into another cylinder, leaving the sediment and a little fluid just above it untouched. The majority of cysts are suspended in the drawn-off portion of the emulsion. Centrifuge the fluid, pour off the supernatant fluid and add water. Centrifuge again. Repeat this three times until the supernatant fluid becomes clear. The sediment will be found to contain more numerous cysts than small sample specimens. Bijlmer (1948) finds the following method the most satisfactory. Suspend a fleck of faeces about the size of a pea in a dish with some 33 per cent ZnS0 4 If much debris appear on the surface, filter through a layer of cheese-cloth. The fluid is decanted into a centrifuge tube, and some more ZnS0 4 solution is added to half a centimeter from
.

the top. After centrifuging for 2 minutes,

lift

a loopful of material

from the surface and place on a

slide.

B. Permanent preparations

Permanent preparations are employed, as was stated before, to supplement, and not to supplant, fresh preparations. Smear preparations are more frequently studied, while section preparations are indispensable in extensive studies of Protozoa. Various fixatives and stains produce different results, care must be exercised in making and evaluating permanent preparations. Diversity of stained objects (Wenrich, 1941).

a.

Smear preparations

Smears are made either on coverglasses or slides. However, coverglass-smears are more properly fixed and require smaller amount of reagents than slide-smears. Greater care must be excerised in handling coverglasses, as they are easily broken. Large free-living Protozoa do not frequently adhere to the glass, since there is not

COLLECTION, CULTIVATION, OBSERVATION

enough albuminous substance
in the culture fluid. If a small
is

895

fresh egg-white emulsified in sterile distilled water

drop of smeared on the coverglass very thinly with the tip of a clean finger, before mounting material for smear, more specimens will adhere to and remain on the coverglass upon the completion of the preparation. Let the smear lie horizontally for 5-10 minutes or longer. Parasitic Protozoa live in media rich in albuminous substances, and therefore, easily adhere to the coverglass in smear. Make uniformly thin smears on coverglasses. If the smears are made from
dysenteric or fluid stools, they should be fixed almost immediately.

Smears made from diarrhoeic or formed stools by emulsifying in warm salt solution, should be left for a few minutes. In any case, do not let the smear become dry except a narrow marginal zone. The smears are fixed next. The most commonly used fixative for Protozoa is Schaudinn's fluid. This is made up as follows:
Cold saturated mercuric
bichloride

(6-7%)

Absolute or

95%

alcohol

66 33

cc.

cc.

Glacial acetic acid

1 cc.

The first two can be kept mixed without deterioration, but the acid must be added just before fixation. Fix at room temperature or warmed to 50C. The fixative is placed in a square Petri dish and the smear is gently dropped on it with the smeared surface facing downward. With a little experience, air bubbles can be avoided and make the smear float on the surface of the fixative. After about one minute, turn it around and let it stay on the bottom of the dish for 5 to 10 more minutes. In case the smear is too thick, a thin coat of vaseline on the upper side of the coverglass will make it to float. About six coverglass-smears may be fixed in the dish simultaneously.

The

coverglass-smears are

now

transferred to a

Columbia staining

jar for coverglasses, containing

50% alcohol for

10 minutes, followed

by two changes
to
is

for similar length of time. Transfer the smears next

30%
now

alcohol for 5 minutes, and then to a jar with water, which

placed under gently running tap water for 15 minutes. Rinse

them

water and stain. Other fixatives frequently used for Protozoa are as follows:
in distilled

Bouin's fluid
Picric acid (saturated)

Formaldehyde
Glacial acetic acid

75 25

cc. cc.

5 cc.

896

PROTOZOOLOGY
70%
alcohol until picric acid

Fixation for 5-30 minutes; wash with

is

completely washed away from the smears.

Sublimate-acetic

Saturated sublimate solution

Glacial acetic acid

100

cc.
cc.
(p. 897).

This

is the original fixative for Feulgen's nucleal reaction Fixation and after-treatment similar to Schaudinn's fluid.

Carnoy's fluid

COLLECTION, CULTIVATION, OBSERVATION

897

washed thoroughly in running water for about 30 minutes. Rinse them in distilled water. Transfer them through ascending series of alcohol (50 to 95%). If counter-staining with eosin is desired, dip the smears which were taken out from 70% alcohol, in 1% eosin in 95% alcohol for a few seconds, and then in 95% plain alcohol. After two passages through absolute alcohol and through xylol, the smears are mounted one by one on a slide in a small drop of mixture of Canada balsam and xylol. The finished preparations are placed in a drying oven at about 60C. for a few days.
Other stains that are often used are as follows:
is diluted to 1:5a slow, but progressive staining which requires no decolorization may be made; but if stock solution is used, stain for 1-16 hours, and decolorize in 0.5% HC1 water or alcohol. If mounted in a neutral mounting medium, the staining remains true for a long time. Mayer's paracarmine. In slightly acidified 70% alcohol solution,

Delafield's haematoxylin. If the stock solution

10,

it is

excellent for staining large Protozoa. If over-stained, decolorize

with 0.5%

HC1 alcohol.
stain.

Giemsa's

Shake the stock solution bottle

well.

By means

of

a stopper-pipette dilute the stock with neutral distilled water (5-10

drops to 10 cc). Smears fixed in Schaudinn's fluid and washed in neutral distilled water are stained in this solution for 10 minutes to 6 hours to overnight. Rinse them thoroughly in neutral distilled water and transfer them through the following jars in order (about 5 minutes in each): (a) acetone alone; (b) acetone: xylol, 8:2; (c) acetone: xylol, 5:5; (d) acetone xylol, 2:8; (e) two changes of xylol. The smears are now mounted in cedar wood oil (which is used for immersion objectives) and the preparations should be allowed to dry for a longer time than the balsam -mounted preparations. Feulgen's nucleal reaction. The following solutions are needed. (a) HC1 solution. This is prepared by mixing 82.5 cc. of HC1 (specific gravity 1.19) and 1000 cc. of distilled water. (b) Fuchsin-sodium bisulphite. Dissolve 1 gm. of powdered fuchsin (basic fuchsin, diamant fuchsin or parafuchsin) in 200 cc. of distilled water which has been brought to boiling point. After frequent shaking for about 5 minutes, filter the solution when cooled down to 50C. into a bottle and add 20 cc. HC1 solution. Cool the solution further down to about 25C. and add 1 gm. of anhydrous sodium bisulphite. Apply stopper tightly. Decolorization of the solution will be completed in a few hours, but keep the bottle in a dark place for at least 24 hours before using it. (c) Sulphurous water:
:

898

PROTOZOOLOGY
Distilled or tap water

200
10

cc.

10% anhydrous sodium

bisulphite
cc. cc.

HC1
ent of chromatin.

solution (a)
is

10

Feulgen's reaction

used to detect thymonucleic acid, a constitucertain purin-bodies in the

Schiff's reaction

By a partial hydrolysis,

acid are split into aldehydes which

show a sharp

upon coming

with fuchsin-sodium bisulphite. Thus this is a reaction, and not a staining method. Smears fixed in sublimateacetic or Schaudinn's fluid are brought down to running water, after being placed for about 24 hours in 95% alcohol. Immerse them in cold HC1 for one minute, then place them in HC1 kept at 60C. (over a microburner or in an incubator) for 5 minutes, quickly immerse in cold HC1. After rapidly rinsing in distilled water, place the smears in solution (b) for 30-minutes to 3 hours. There is no overstaining. The smears are then washed in three changes (at least 2 minutes in each) of solution (c). Wash them in running water for 30 minutes. If counterstaining is desired, dip in 0.1% light green solution and rinse again in water. The smears are now dehydrated through a series of
in contact

alcohol in the usual

manner and mounted

in

Canada balsam

(Feul-

gen and Rossenbeck, 1924; Feulgen-Brauns, 1924; Feulgen, 1926; Coleman, 1938; Stowell, 1945). Silver-impregnation methods. Since Klein (1926) applied silver nitrate in demonstrating the silver-line system of ciliates, various modifications have been proposed. Dry silver method (Klein, 1926). Air-dried cover glass smears are placed for 6-8 minutes in a 2 per cent solution of silver nitrate and thoroughly washed. The smears are exposed to sunlight for 2-8 hours in distilled water in a white porcelain dish, with occasional control under the microscope. The smears are then washed thoroughly and air-dried; finally mounted in Canada balsam. Wet silver method (modified after Gelei and Horvath, 1931). The ciliates are fixed in a centrifuge tube for 5-10 minutes in sublimateformaldehyde solution, composed of saturated corrosive sublimate 95 cc. and formaldehyde 5 cc. The specimens are now washed twice in nonchlorinated water and once in distilled water; they are then treated in 1.5-2 per cent solution of silver nitrate for 5-20 minutes.

Without washing, the specimens

in the

tube are exposed to direct

sunlight for 10-60 minutes in distilled water, after which the speci-

mens

are

washed 4-6 times

in distilled water,

one minute each. Pass-

ing through a gradually ascending alcohol series and xylol, the speci-

mens

are

mounted

in

Canada balsam.

COLLECTION, CULTIVATION, OBSERVATION

899

Fontana's method. For staining filamentous structures such as the extruded polar filament of microsporidian spores, this method is the most satisfactory one. After air-drying the smears are fixed for 5 minutes in a mixture of formaldehyde, 20 cc; glacial acetic acid, 1

cc; and distilled water, 100 cc. After washing in running water, the smears are placed in the following mordant composed of equal parts

and 1 per cent carbolic acid, for about 2 minutes at about 60C. Wash the smears in water and place them for 3-5 minutes in 0.25 per cent solution of silver nitrate warmed to 60C, to which ammonia has been added drop by drop until a grayish brown cloud appeared. Wash thoroughly and air-dry. After passing through 95 per cent and absolute alcohol, and xylol, the smears are mounted in Canada balsam
of 5 per cent tannic acid
b.

Blood film preparations

is cleaned with 70% alcohol. with an aseptic blood lancet or a sterilized needle. Wipe off the first drop with gauze and receive the second drop on a clean slide about half an inch from one end (Fig. 376, 1). Use care not to let the

Thin

film.

The

finger tip or ear lobe

Prick

it

slide touch the finger or ear-lobe itself. Quickly bring a second slide, one corner of which had been cut away, to the inner margin of the blood drop (1), and let the blood spread along the edge of the second slide. Next push the second slide over the surface of the first slide at an angle of about 45 toward the other end (#). Thus a thin film of blood is spread over the slide (3). Let the slide lie horizontally and dry, under a cover to prevent dust particles falling on it and to keep away flies or other insects. If properly made, the film is made up of

a single layer of blood

cells.

Often parasites are so few that to find them in a thin film involves a great deal of time. In such cases, a thick film is advocated. For this, 2 to 4 drops of blood are placed in the central halfinch square area, and spread them into an even layer with a needle or with a corner of a slide. Let the film dry. With a little practice, a satisfactory thick smear can be made. It will take two hours or more to dry. Do not dry by heat, but placing it in an incubator at 37C. will hasten the drying. When thoroughly dry, immerse it in water and dehaemoglobinize it. Air dry again.
films.

Thick

Thin and thick film. Often it is time-saving if thin and thick films made on a single slide. Place a single drop of blood near the center and make a thin film of it toward one end of the slide. Make a small thick smear in the center of the other half of the slide. Dry. When
are

900

PROTOZOOLOGY

thoroughly dry, immerse the thick film part in distilled water and dehaemoglobinize it. Let the slide dry. Blood smears must be stained as soon as possible to insure a proper staining, as lapse of time or summer heat will often cause poor staining especially of thick films. Of several blood stains, Giemsa's and Wright's stains are used here. For staining with Giemsa's stain, the thin film is fixed in absolute methyl alcohol for 5 minutes. Rinse well

Fig. 376.

Diagrams showing how a thin blood

film is

made on

a slide.

the slide in neutral distilled water. After shaking the stock bottle (obtained from reliable makers) well, dilute it with neutral distilled water in a ratio of one drop of stain to 1-2 cc. of water. Mix the solu-

and the blood film is placed in it for 0.5-2 hours or longer if needed. Rinse the slide thoroughly in neutral distilled water and wipe off water with a tissue paper from the underside and edges of the slide. Let the slide stand on end to dry. When thoroughly dry,
tion

place a drop of xylol and a drop of cedar

objectives)

and cover with a

coverglass.

wood oil (used for immersion The mounting medium

COLLECTION, CULTIVATION, OBSERVATION

should be absolutely neutral.
ing, as acid in it

901

Do

not use Canada balsam for mount-

promptly

spoils the staining.

For Wright's stain, fixation is not necessary. With a medicine dropper, cover the dried blood film with drops of undiluted Wright's stain, and let the film stand horizontally for 3-5 minutes then the
;

same number of drops of neutral distilled water is added to the stain and the whole is left for 10-30 minutes. The stain is then poured off and the film is rinsed in neutral distilled water. Dry. Mount in xylol and cedar wood oil. Use of coverglass on a stained blood film is advocated, since a cedar wood oil mounted slide allows the use of dry objectives which in the hand of an experienced worker would give enough magnification for species determination of Plasmodium, and which will very clearly reveal any trypanosomes present in the film. Furthermore, the film is protected against scratches, and contamination by many objects which may bring about confusion in detecting looked-for
organisms.

Films made from splenic punctures for Leishmania or Trypano-

soma

are similarly treated

c.

and prepared.

Section preparations

Paraffin sections should be

made according
same

to usual histological

technique. Fixatives and stains are the

as those

mentioned for

smear preparations.
References

Balamuth, W.:

(1951) Biological studies on Entamoeba histolytica.

III. J. Infect. Dis.,

88:230.

and Sandza, J. G.: (1944) Simple, standardized culture medium for physiological studies on Entamoeba histolytica. Proc. Soc. Exper. Biol. Med., 57:161. Bass, C. C. and Johns, F. M.: (1912) The cultivation of malarial Plasmodia (Plasmodium vivax and P. falciparum) in vitro. J.
Exper. Med., 16:567.

Becker, E. R.: (1926) Endamoeba citelli, etc. Biol. Bull., 50:444. Belar, K.: (1928) Untersuchungen der Protozoen. Methodik. wiss.
Biol., 1.

Bijlmer,

J.: (1948) On the recovery of Protozoa and eggs of some species of helminths in human faeces. J. Parasitol., 34:101. Boeck, W. C. and Drbohlav, J.: (1925) The cultivation of Enda-

moeba histolytica. Am. J. Hyg., 5:371. Chatton, E. and Brodsky, A.: (1909) Les parasitisme d'une ChyArch. Protist., 17:1. tridine du genre Sphaerita, etc.
Claff, C. L.: (1940)
migration-dilution apparatus for the sterilization of Protozoa. Physiol. Zool., 13:334.

902

PROTOZOOLOGY
L. R.
:

P.: (1930) Encystation, mulwithout encystment, etc. Arch. Protist., 70:223. Coleman, L. C. (1938) Preparation of leuco basic fuchsin for use in the Feulgen reaction. Stain Tech., 13: 123. Dobell, C. and Laidlaw, P. P.: (1926) On the cultivation of Entamoeba histolytica and some other entozoic amoebae. Parasitoltiple fission

Cleveland,

and Sanders, Eliz.

ogy, 18:283.

Feulgen, R.: (1926) Die Nuclealfarbung. Abderharden's Handb.

biol.

Arbeitsmeth., Abt.

5,

2:1055.

and Rossenbeck, H.: (1924) Mikroskopisch-chemischer Nachweis einer Nucleinsaure von Typus der Thymonucleinsaure und die darauf beruhende elektive Farbung von Zellkernen in mikroskopischen Praparaten. Ztschr. physiol. Chem.,
135:203. iiber Nuclealfarbung. Pfliiger's Arch, gesamt. Physiol., 203:415. Geiman, Q. M., Anfinsen, C. B. et al.\ (1946) Studies on malarial parasites. VII. J. Exper. Med., 84:583. Gelei, J. v. and Horvath, P.: (1931) Eine nasse Silber-bzw. Goldmethode fur die Herstellung der reizleitenden Elemente bei den Ciliaten. Ztschr. wiss. Mikr., 48:9. Glaser, R. W. and Coria, N. A.: (1930) Methods for the pure culture of certain Protozoa. J. Exper. Med., 51:787. Grasse, P. P.: (1926) Contributions a l'etude des flagelles parasites. Arch. zool. exper. gen., 65:345. Hahnert, W. F.: (1932) Studies on the chemical needs of Amoeba proteus: a cultural method. Biol. Bull., 62:205. Hall, R. P.: (1937) Growth of free-living Protozoa in pure cultures. In Needham et al. : Culture methods for invertebrate animals. (1941) Food requirements and other factors influencing growth of Protozoa in pure cultures. In Calkins and Summers'

Feulgen-Brauns, Frieda: (1924) Untersuchungen

Protozoa

in biological research.

J.: (1921) The cultivation of Trichomonas hominis. Trop. Med., 1:211. (1922) A study of Trichomonas hominis, its cultivation, etc. Bull. Johns Hopkins Hosp., 33:437. Htjtner, S. H. and Provasoli, L.: (1951) The phytoflagellates. In: Lwoffs Biochemistry and physiology of Protozoa. 1. Jahn, T. L.: (1933) On certain parasites of Phacus and Euglena: Sphaerita phaci, sp. nov. Arch. Protist., 79:349. Johnson, J. G. and Trtjssell, R. E.: (1943) Experimental basis for the chemotherapy of Trichomonas vaginalis infestations. Proc. Soc. Exper. Biol. Med., 54:245. Kidder, G. W.: (1941) The technique and significance of control in protozoan culture. In: Calkins and Summers' Protozoa in bio-

Hogue, Mary

Am.

J.

logical research.

Dewey, Virginia C. and Parks, R. E. Jr.: (1951) Studies on inorganic requirements of Tetrahymena. Phvsiol. Zool., 24:
69.

Kirby, H. Jr.: (1941) Organisms living on and in Protozoa. In Calkins and Summers' Protozoa in biological research.

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(1950) Materials and methods in the study of Protozoa. Berkeley, California. Klein, B. M.: (1926) Ergebnisse mit einer Silbermethode bei CiliaArch. Protist., 56:243. ten. Marsland, D. A.: (1943) Quieting Paramecium for the elementary student. Science, 98:414. Mattes, O.: (1924) Ueber Chytridineen im Plasma und Kern von Amoeba sphaeronucleus und A. terricola. Arch. Protist., 47:413. Needham, J. G., Galtsoff, P. S., Ltjtz, F. E. and Welch, P. S.: (1937) Culture methods for invertebrate animals. Ithaca, N. Y. Pringsheim, E. G.: (1926) Kulturversuche mit chlorophyllflihrenden Mikroorganismen. V. Beitr. Biol. PH., 14:283. (1937) Beitrage zur Physiologie saprotropher Algen und Planta, 27:61. Flagellaten. III. (1946) Pure cultures of algae. Cambridge. Ratcliffe, H. L. and Geiman, Q. M.: (1938) Spontaneous and experimental amoebic infection in reptiles. Arch. Path., 25:160.
die Vermehrung von Blastocystis in der Kultur. Arch. Protist., 92:226. Sassuchin, D. N.: (1928) Zur Frage iiber die Parasiten der ProtoIbid., 64:61. zoen. Popoff, P. P., Kudrjewzew, W. A. and Bogenko, W. P.: (1930) Ueber parasitische Infektion bei Darmprotozoen. Ibid., 71:229. Spingarn, C. L. and Edelman, M. H.: (1947) The prolongation of the viability of cultures of E. histolytica by the addition of streptomycin. J. Parasitol., 33:416. Stowell, R. E.: (1945) Feulgen reaction for thymonucleic acid. Stain Tech., 20:45. Taylor, C. V. and Van Wagtendonk, W. J.: (1941) Growth studies Physiol. Zool., 14:431. of Colpoda duodenaria. I. Tobie, Eleanor J., von Brand, T. and Mehlman, B.: (1950) Cultural and physiological observations on Trypanosoma rhodeJ. Parasitol., 36:48. siense and T. gambiensc. Trager, W. (1934) The cultivation of a cellulose-digesting flagellate, Trichomonas termopsidis, and of certain other termite Protozoa. Biol. Bull., 66:182. (1950) Studies on the extracellular cultivation of an intraJ. Exper. Med., 92:349. cellular parasite (avian malaria). I. Wenrich, D. H.: (1941) The morphology of some Protozoan parasites in relation to microtechnique. J. Parasitol., 27:1. Wenyon, C. M.: (1926) Protozoology. London and Baltimore. Wichterman, R. (1949) The collection, cultivation, and sterilizaProc. Perm. Acad. Sc, 23:151. tion of Paramecium.

Reyer, W.: (1939) Ueber

Author Index
Aberle, S. D., 612, 626 Adams, A. R. D., 450, 451, 471, 887 Adams, J. A., 548, 566 Adamson, A. M., 331 Adler, S., 355, 365 Ahlstrom, E. H., 265, 270 Alden, R. H., 101, 138

Barrera, A., 618, 632 Barret, H. P., 15, 16, 458, 466, 886,

889
Bartlett, D. E., 388, 398 Bary, B. M., 107, 136, 706, 720 Bass, C. C., 889, 901 Basu, S. P., 649, 664 Bayon, H. P., 336, 338 Beauchamp, P. d., 721 Becker, E. R., 105, 136, 335, 338, 353, 354, 365, 390, 398, 403, 466, 576, 577, 579, 580, 594, 595, 596, 598, 617, 626, 817, 818, 821, 822, 826, 828, 893, 901 Beers, C. D., 91, 110, 136, 150, 153, 175, 176, 177, 178, 209, 214, 698, 704, 720, 747, 754, 758, 772, 779, 787, 798, 811 Behrend, K., 150 BSlaf, K., 44, 91, 156, 163, 166, 167, 168, 175, 205, 207, 208, 209, 214, 362, 365, 371, 398, 407, 414, 480, 491, 507, 515, 573, 595, 881, 883, 901 Belda, W. H., 117, 120, 136, 141, 442 446, 883 Belkin, M., 105, 106, 137 Bellerive, A., 606, 632 Beltran, E., 685, 688, 803, 811 Bennett, S. C. J., 230, 244 Ber, M., 355, 365 Berenberg-Gossler, H., 629 Berlin, H., 531, 566 Bernheimer, A. W., 241, 243 Bernstein, T., 117, 139, 404, 414 Berthold, C, 122, 136 Bhatia, B. L., 533, 534, 566, 685, 688 Biggar, Ruth B., 750, 800, 811

Alexander, G., 26
Alexeieff, A., 80, 91, 390, 397, 640,

641
Allee, W. C, 112, 136 Allegre, C. F., 297, 307, 545, Allen, Ena A., 594 Allen, W. E., 327, 329

566

Allman, G. J., 16, 75 Altenberg, E., 241, 243 Alvey, C. H., 102, 138

Amberson, W. R., 117, 136 Andai, G., 371, 397 Anderson, A. P., 355, 367 Andresen, N., 82, 106, 107, 115, 116 121, 136, 442, 466 Andrews, Bess J., 404, 414 Andrews, E. A., 808, 809, 811
Andrews, J., 388, 395, 397, 403, 579, 582, 594 Andrews, J. M., 607, 626 Andrews, Mary N., 387, 398 Anfinsen, C. B., 889, 902 Angerer, C. A., 437, 466 Anigstein, L., 713, 720 Aragao, H. B., 283, 290, 594, 619 Arantes, J. B., 625, 626
Arcichovskij, V., 46, 91 Aris, F. W., 606, 627 Arndt, A., 156 Atchley, F. O., 622, 626, 889 Auerbach, M., 643, 649, 657, 663 Awerinzew, G. W., 859, 861 Awerinzew, S., 663, 820 826
;

Bijlmer,

J.,

901

B
Babudieri, B., 639, 641 Baker, H., 11, 16

Balamuth, W., 176, 213, 452, 466, 811, 888, 889, 901 Balbiani, G., 13, 14, 16 Balech, E., 299, 307, 312, 329, 816,
826
Ball, G. H., 547, 560, 566 Bancroft, M. J., 665 Baraban, L., F 639, 641 Barbagallo, P., 466 Barker, H. A., 175, 178, 213, 222 Barksdale, W. L., 586, 594 Barnes, W. B., 388, 398

Bischoff, A. L., 620, 629 Bishop, Ann, 167, 336, 338, 386, 390, 398, 459, 463, 466, 615, 626 Bishop, E. L. Jr., 854, 861 Blattner, H., 129, 130, 136, 803, 811 Blanc, G., 625, 628 Bland, P. B., 26, 35 Bliznick, A., 582, 595 Bloom, W., 602, 630 Boeck, W. C., 16, 167, 374, 375, 398, 447, 450, 451, 887, 901 Bodine, J. H., 175, 214 Boell, E. J., 196, 197, 214 Bohm, A., 326, 330

Bogenko, W.

P.,

903

Bold, H. C., 282, 283, 284, 288, 290 Boley, L. E., 401

Bond, F.

F., 658,

663

Borchert, A., 679

905

906

PROTOZOOLOGY
Cannon,
P. R., 615, 628 Cantrell, W., 602, 630 Carini, A., 459, 466, 663, 685, 688, 800, 811 Carr, H. P., 606, 628

Borgert, A., 163, 168, 326, 330, 525 Botsford, Emily F., 119, 136 Boughton, D. C, 577, 585, 586, 595 Boughton, Ruth B., 585, 595 Bowling, R. C, 207, 215, 566 Boyd, M. F., 32, 226, 600, 602, 604, 605, 606, 607, 608, 609, 626, 627 Bozler, E., 136, 743, 754 Brachet, J., 212, 214 Brackett, S., 582, 595 Brady, B. H., 504

Braem,

F., 679 Brandly, C. A., 388, 401 Brandt, K., 102, 212, 516, 524 Bremer, H., 168, 655, 663 Brent, M. M., 452, 466 Bresslau, E., 55, 91, 747 Bretschneider, L. H., 817, 827 Breuer, R., 491 Brodsky, A., 74, 91, 893, 901 Brown, E. M., 321, 330 Brown, H. P., 53, 54, 91 Brown, J. A., 597 Brown, V. E., 63, 78, 79, 91, 406, 410, 414 Bruce, D., 14, 16 Brug, S. L., 101, 136, 614, 628

Casagrandi, O., 466 Cash, J., 425, 466, 491, 506, 515 Catanel, A., 633 Caullery, M., 641, 663 Cavallini, F., 859, 861 Cpede, C, 649, 664, 691, 698 Cerny, W., 618, 620, 628 Chadefoud, M., 81, 91 Chagas, C, 166, 467 Chakravarty, M., 566, 586, 595, 649, 664 Chalkley, H. W., 20, 35, 135, 139, 169, 215, 216, 437, 466, 882 Chambers, R., 22, 35, 870, 878 Chang, S. L., 451 Chatterjee, G. B., 533, 534, 566 Chatton, E., 56, 66, 74, 76, 92, 167,
213, 215, 228, 312, 321, 330, 625, 628, 678, 679, 721, 735, 754, 774, 776, 781, 782, 783, 784, 785, 786, 787, 789, 795, 844, 845, 893, 901 Cheissin, E., 691, 698, 779, 787 Chen, T. T., 154, 166, 168, 189, 194, 195, 196, 202, 215, 221, 459, 467, 470, 616, 628, 688, 689 Chen, Y. T., 53, 54, 55, 92, 100, 101, 105, 133, 137, 304, 307 Chernin, E., 622, 628 Christensen, J. F., 579, 595, 817, 828 Christiansen, Elizabeth B., 167, 401

Buddenbrock, W.
744

E., 349, 365, 617, 628, 799, 811, 826, 827 v., 170, 214 Butschli, O., 13, 14, 16, 112, 122, 126, 136, 187, 214, 253, 269, 663, 688,

Brumpt,

Bullington, W. E., 128, 129, 136, 742, 754, 758, 772, 843, 845 Bundesen, H. N., 449, 466 Bunting, Martha, 371, 398 Buonanni, F., 11, 16 Burbank, W. D., 762, 772 Burk, Myrle, 433, 434

Cienkowski,

L., 425 Claff, C. L., 104, 109, 137, 140, 150,

176, 214, 218, 754, 755, 772, 884,

Burks, C, 466 Burnside, L. H., 213, 214, 806 Burroughs, R. D., 176, 218 Burt, R, L., 66, 91, 150, 214, 745, 747,

754 Busch, W., 816, 826 Buschkiel, Marianne, 566 Bush, Mildred, 694, 698, 788, 817, 826 Butcher, A. D., 710, 720 Butterfield, Winifred, 197, 220

901 Claparede, J., 12, 16 Clark, A. M., 117, 137, 212, 215 Clarke, C. H. D., 617, 622, 628 Clarke, D. H., 617, 628 Clegg, M. T., 15, 18, 883 Cleveland, L. R., 8, 16, 29, 34, 35,
42, 77, 92, 99, 105, 106, 118, 136, 159. 160, 167, 168, 170, 185, 215,

Calkins, G. N.,

6, 13, 16, 44, 45, 82, 97, 136, 146, 149, 163, 169, 176,187, 190, 206, 207, 209, 214, 228, 243, 265, 318, 330, 566, 704, 717, 720, 769, 806, 814, 835, 843, 845, 865 Callender, G. R., 633 Calvez, J. le., 496, 504 Campbell, A. S., 63, 751, 754, 816,

828
Canella,

M.

F., 727,

735

216, 226, 243, 378, 379, 380, 389, 398, 404, 409, 411, 412, 414, 415, 447, 458, 467, 744, 754, 888, 902 Coatney, G. R., 351, 367, 592, 598, 614, 615, 618, 620, 628, 631 Coggeshall, L. T., 22, 36, 602, 606, 607, 614, 617, 627, 628, 631, 634 Cohn, F. J., 12, 16 Cohn, L., 655, 664 Cole, F. J., 16 Coleman, L. C, 898, 902 Collier, Jane, 92, 137, 216, 398, 415 Collin, B., 60, 172, 253, 780, 878 Conklin, C, 691, 698 Connal, A., 585, 595 Connell, F. H., 63, 150, 378, 398, 788

AUTHOR INDEX
Conolly, G.
I.,

90<

466

Conrad, W., 257, 258, 259, 260, 267,

270, 279, 290, 297, 299, 307, 320, 321, 330 Cook, W. R. I., 433, 434 Cordero, E. H., 656, 664 Coria, N. A., 21, 36, 884, 902 Corliss, J. O., 760, 772 Cosmovici, N. L., 102, 137 Coulston, F., 602, 630 Coventry, F. A., 351, 365 Craig, C. F., 449, 467 Crawley, H., 350, 365, 543, 551, 555, 566, 641, 827 Crouch, H. B., 577, 580, 594, 595

Crow, W.

B.,

290

Crump, Lettice M., 176, 178, 216 Culbertson, J. T., 33, 36 Cull, S. W., 187, 190, 215 Cupp, Easter E., 167
Curtis, W. C, 744, 754 J. A., 47, 92, 496, 504 Cutler, D. W., 15, 16, 176, 215, 410,

Cushman,

415 Czurda, V., 90

da Cunha, A. M., 307, 649, 664, 735,

800, 804, 811, 812, 827

da Cunha, A. X., 860, 861 da Fonseca, O. O. R., 377, 398, 649, 664
Dallinger,

W.

Dangeard, P. 893

H., 21, 36 A., 167, 291, 308, 467,

Daniel, G. E., 135, 137, 169, 215, 216, 466 Daniels, E. W., 135, 137, 442, 467 Darby, H. H., 26, 27, 36, 17 5,216 Darling, S. T., 351, 365, 605, 628,
639, 641

Das-Gupta, M., 817, 827

M. S., 151, 216 Davaine, C. J., 14, 16 Davies, D. M., 622, 629 Davis, Betty S., 351, 365 Davis, H. S., 167, 372, 393, 398,
Dass, C.
,

467, 648, 649, 652, 654, 664,

878
Davis, T. G., 169, 216, 824, Dawson, J. A., 101 105,
153, 177, 216, 437, 467

de Bary, A., 429, 434

De

Garis, C. F.,
la

191, 216,

243

De

Arena, Debaisieux,

J. F., 104,

137

P., 154, 168, 645, 655, 657, 660, 664, DeCoursey, J. D., 670, 681 Deeds, O. J., 583, 595 Deflandre, G., 267, 270, 476, 484, 491

908

PROTOZOOLOGY
E
Foyn,

Earle,

W. C,

606, 628

Eddy, S., 312, 330 Edelman, M. H., 889, 903

Edgar,
S. A., 113,
J. J.,

B., 476, 491 Foner, A., 586, 596 Fortner, H., 120, 138 Foster, A. O., 582, 596

Edwards,
Efimoff,

137 101

Fott, B., 167, 306, 308

Franz, V., 253

Fraser, L. A., 137 Frenz, O., 579, 597 Frisch, J. A., 25, 36, 118, 138 Fritsch, F. E., 270, 271, 275, 308, 330

22, 36 Ehrenberg, C. G., 12, 17

W. W.,

Eichhorn, J. C, 11, 17 Eimer, T., 14, 17 Eisenberg, E., 119, 137 Elkeles, G., 348, 365 Elliott, A. M., 106, 167, 277, 291 Elliott, E. W., 434 Ellis, J., 11, 17, 75 Ellis, M. M., 543, 552, 556, 566 Emik, L. O., 99, 138

291,

Frosch, P., 217 Froud, Joan, 836, 845 Fry, W. E., 626, 633 Frye, W. W., 226, 243, 453, 577, 594, 888

450,

452,

Emmerson, M.
817, 826

A.,

136,

388,

403,

Emmet,

J., 134, 138 Engel, Fr., 106, 136 Engelmann, T. W., 63, 102, 138 Engley, F. B., 402 Enriques, P., 169, 206, 209, 216 Entz, G., 176, 217, 281, 291, 326,

Fujita, T., 649, 664 Fuller, H. S., 357, 365 Fulton, J. D., 605, 632 Fulton, J. F. Jr., 859, 860, 861 Furgason, W. H., 225, 243, 747, 756, 760, 772 Furssenko, A., 857, 861 Fyg, W., 670, 680

330, 371, 464, 467

Erdmann, Rhoda,

151, 222, 655,

664

Evans, F. R., 178, 218, 748, 755 Everritt, Martha G, 217

Galli-Valerio, B., 390, 399 Galtsoff, P. S., 38, 311, 330, 560, 567,

903

Garnham,
629, 633

P.

C,

602, 603, 604,

Fabyan, M., 337, 338

Fair, G. M., 451 Fallis, A. M., 616, 622, 628, 629 Fantham, H. B., 649, 664, 671, 672,

Garnjobst, L., 175, 217

Gatenby,

J. B., 79,

303, 308

Gates, G. E., 566

Gaw, H.

680
Farber, S. M., 390, 402 Farkas, B., 876, 878 Farrar, C. L., 670, 680 Faure, Alice, 390, 399

841, 845 Gaylord, H. R., 21, 36 Geckler, R. P., 239, 243 Gehenio, P. M., 22, 38 Geiman, Q. M., 357, 365, 374, 399,
Z., 120, 138,

Faure-Fremiet, E., 28, 36, 82, 113,

138, 213, 217, 690, 698, 721, 725, 735, 761, 763, 795, 856, 859, 860, 861, Fedorowa, T., 817, 827 Feo, L. G., 387, 399, 402 Ferber, K. E., 817, 827 Fernandez, D. F.-G., 687,

453, 459, 467, 470, 609, 629, 706, 721, 804, 812, 887, 889, 902, 903
Geitler, L., 90, 92, 282, 291, 326, 330,

713, 714, 769, 772, 865, 878

365
Gelei, G. v., 84, 138, 765, 772 Gelei, J. v., 56, 66, 68, 92, 101, 119, 138, 725, 735, 742, 743, 755, 898,

902
689, 817,

827 Fernandez-Galiano, D., 806, 811 Ferrebee, J. W., 609, 629 Feulgen, R., 898, 902 Feulgen-Brauns, Frieda, 898, 902 Fiebiger, J., 584, 595 Fiene, A. R., 403 Filice, F. P., 393, 399 Finley, H. E., 24, 36, 118, 169, 178, 199, 217, 855, 856, 861, 862 Fischer, A., 53, 92
Fish, F. F., 579, 580, 582, 595, 649,

Georgevitch, 665

J., 35, 36,

168, 649, 658,

Gerloff, J., 277, 291 Giese, A. C, 46, 92,

101,

138,

192,

202, 217, 803

H. P. S., 606 Gilman, L. C, 192, 217 Gilmore, H. R., Jr., 640, 641
Gillette,

664
Foa, Anna, 397, 399, 406, 410, 416,

Glaessner, K., 106 Glaser, R. W., 21, 36, 350, 354, 365, 884, 902 Gluge, G., 14, 17 Gohre, E., 112, 138, 528, 566 Gonnert, R., 864, 865, 878

Goethard, 317
Goette, A., 483, 491

AUTHOR INDEX
Goidics, Mary, 294, 308 Go'ldfuss, G. A., 11, 17 Goldstein, L., 35 Golgi, C, 14, 17, 66

909

Hale, H. P., 22, 35 Hall, C. E., 53, 56, 73, 93

Hall, Phoebe R., 594 Hall, R. P., 26, 79, 80, 81, 92, 97, 102, 112, 138, 166, 167, 170, 217, 303, 304, 308, 314, 326, 330, 839, 845, 856, 884, 902 Hall, S. R., 16, 92, 137, 216, 398, 404, 415 Haller, E. v., 349, 365 Hamilton, J. M., 808, 812 Hammond, D. M., 66, 92, 577, 596, 841, 845 Hardcastle, A. B., 577, 584, 596 Hardin, G., 25, 28, 36, 343, 366, 744,

Gonder, R., 629 Goodey, T., 423, 425 Goodrich, E. S., 539, 567 Goodrich, Helen P., 528, 538, 539, 547, 550, 567 Goodrich, J. P., 874, 878 Goor, A. C. J. Van, 318, 330 Gordienko, M., 299 Graham, H. W., 330 Granata, L., 661, 663, 665
Grasse, P. P., 35, 36, 77, 79, 80, 82, 92, 138, 157, 217, 269, 341, 344, 362, 365, 370, 374, 376, 379, 385, 390, 399, 406, 407, 408, 409, 415, 685, 689, 893, 902 Grassi, B., 391, 399, 405, 406, 409, 410, 412, 414, 415, 416, 605
127, 129, 138 Greeff, R., 106, 138, 441, 467 Greeley, A. W., 22, 36 Greenwood, Marion, 102, 138 Gregory, Louise H., 169, 206,

755 Harding, J. P., 120, 137 Hardy, A. V., 449, 467 Harper, R. A., 291
J., 11, 17 Harrison, J. A., 241, 243 Harting, 11

Harris,

Gray,

J.,

Hartman, E., 615, 629 Hartmann, M., 166, 210,

747,

217, 287, 290, 291, 350, 366, 443, 467

Hartog, M., 106

755
Greiner,
Grell,
J.,

168

K. G., 563, 567 Gremsbergen, C., 117

M., 176, 221, 756 Grocott, R. G., 626, 631 Groot, A. A. de, 440, 467 Gros, G M 14, 17, 456 Gross, F., 317, 330 Grosse-Allerman, W., 212
Griffin, A.

Harvey, E. N., 114, 138, 318, 330 Hassanein, M. H., 32, 37, 670, 680 Hatt, P., 558, 560, 567 Hauschka, T. S., 168, 207, 217, 227, 243, 590 Hawes, R. S., 167, 387, 399 Hawkins, P. A., 596 Haye, A., 87, 93 Hayes, M. L., 44, 73, 93, 149 Hegner, R. W., 8, 17, 212, 225, 243,
364, 366, 393, 395, 399, 461, 468, 491, 614, 615, 625, 629, 686, 689, 735, 798, 812, 883

Gruber, A., 212, 717, 747

Gruby, D.,

14, 17 Gruithuisen, F. v., 11 Giinther, F., 294, 308 Guido, V. M., 25, 38 Guilcher, Yvette, 217, 847, 849, 863,

878 Guimaraes,

Heidenhain, M., 44 Heidenreich, E., 691, 698 Heidt, K., 113, 138 Heinsius, 317

J. R. A., 649, 665 Gulati, A. N., 685, 688 Gurley, R. R., 649, 665 Guthrie, Mary J., 744, 754 Gutierrez-Ballesteros, E., 467

Hemming,
Henderson,

F., 444, 468 J. C., 445, 468

Henneguy, G., 372, 807 Henry, Dora P., 543, 545, 579, 580, 582, 586, 596
Herfs, A., 93, 118, 138 Herman, C. M., 615, 617, 620, 629, 631, 634 Herrick, C. A., 137 Herrlich, A., 586, 596 Hertel, E., 133 Hertwig, R., 44, 93, 190, 204, 217, 519

H
Haagen-Smit, A. J., 178, 217, 222 Haas, G., 709, 721 Haase, A., 582, 596 Hackett, L. W., 605, 629
Haeckel, E. H., 5, 525 Haecker, V., 525
12, 17, 39, 61, 92,

525
Hesse, E., 535, 567, 584, 590, 596, 658, 666, 669, 670, 676, 677, 680, 681 Hester, H. R., 401

Hagelstein, R., 430, 434

Hager, Anna, 595 Hahnert, W. F., 882, 902

Hake, T. G., 13, 17 Hakansson, E. G., 226, 245

Halberstaedter, L., 134, 138

Hetherington, A., 27 Hetherington, D. C, 674, 681 Hewer, H. R., 82

910

PROTOZOOLOGY
Ilowaisky, S. A., 178, Inman, O. L., 133 Ito, T., 464, 468

Hewitt, D. C, 177, 216 Hewitt, R., 468, 615, 620, 629 Hickson, S. J., 684 Hieronymus, G., 185 Higgins, Helen T., 805, 812
Hill, J., 11, 17 Hill, R. B., 606,

217

Ivanic, M., 145, 169, 176, 218, 335, 366, 487, 491, 732, 735

628 Hinshaw, H. C, 167, 217 Hinshaw, W. R., 377, 393, 401 Hirschfield, H. I., 134, 141, 859, 861
Hirschler, J., 79 Hiwatashi, K., 192, 197, 217 Hoare, C. A., 230, 244, 457, 468, 824, 827 Ilofeneder, H., 326, 330, 341 Hofker, J., 318, 330, 816, 827 Hogan, M. J., 626, 629
J., 118, 138, 364, 366, 387, 388, 399, 468, 885, 902 Hollande, A., 76, 93, 257, 270, 273, 274, 275, 276, 281, 291, 293, 294, 303, 304, 306, 308, 362, 366, 370, 399, 441, 468 Holmes, F. O., 354, 366, 470 Holter, H., 104, 106, 107, 115, 121, 136, 138 Honess, R. F., 579, 596 Honigberg, B., 363, 366, 389, 400 Hoogenraad, H. R., 472, 480, 486,

J Jacob, V. P., 606, 632 Jacobs, D. L., 321, 330 Jacobs, L., 626, 630 Jacobson, Irene, 66, 70, 93 Jaczo, I., 649, 665 Jahn, E., 429, 434 Jahn, T. L., 21, 26, 37, 106, 118, 139, 293, 297, 303, 307, 308, 583, 595, 649, 667, 854, 861, 862, 874, 878,
894, 902 Jahoda, Posa, 277, 292 Jakubowska, Wanda, 861 Jakus, Marie A., 53, 56 ,73, 93 James, S. P., 600, 602, 607, 630 Jameson, A. P., 168, 208, 218, 567, 649, 665, 670, 680, 735, 799, 812 Janda, Y, 34, 37, 676, 677, 680 Janet, C, 291
Janicki, C, 77, 93, 167, 397, 399, 407, 416, 466, 468

Hogue, Mary

Jaquette, D.
Jarocki,
J.,

S.,

641

774, 779, 783, 784, 787,

491 Hopkins, D. L., 104, 139 Horning, E. S., 80, 81, 82, 93, 95
133, 139, 154, 217, 832, 845, 898, 902 Houlihan, R. K., 106, 143 Houwink, A. L., 54, 93, 94 Hovasse, R., 109, 142, 250, 253, 324, 330, 699 Howland, Ruth, 26, 37, 46, 93, 104, 117, 139 Hsiung, T. S., 335, 338, 399, 717, 719, 721, 750, 753, 755, 824, 826, 827,
J.
v.,

861
Jefferey, G. M., 617, 630

Jennings, H.

Horvath,

S., 7, 13, 18, 122, 130, 131, 132, 135, 139, 192, 194, 196, 206, 210, 211, 218, 225, 229, 244, 484, 491, 744, 755, 802

Jensen, P., 132 Jepps, Margaret W., 226, 243, 418, 425, 462, 468, 473, 491, 694, 699 Jickeli, C. F., 202, 218
Jirovec, O., 34, 37, 55, 66, 93, 115, 139, 663, 665, 670, 674, 676, 677, 678, 680 Joblot, L., 11, 18 Johns, F. M., 889, 901 Johnson, D. F., 26, 301, 308 Johnson, G., 386, 402 Johnson, H. P., 591, 598 Johnson, J. G, 885, 902 Johnson, L. P., 90, 294, 297, 308 Johnson, P. L., 437, 440, 469 Johnson, W. H., 178, 218, 748, 755 Johnston, T. H., 665 Johnstone, H. G., 456, 468 Jollos, Y, 45, 227, 228, 229, 244,442, 443, 468, 476, 491 Jones, A. W., 567 Jones, E. E. Jr., 727, 735 Jones, E. P., 27 Jones, F. E., 626, 630 Jones, P. M., 433, 434 Joyet-Lavergne, Ph., 79, 82 Joyeux, C, 826, 827 Jung, \Y, 490, 491

873
Huff, C. G., 246, 602, 604, 615, 616, 617, 618, 620, 622, 629, 630, 632, 633, 878 Huizinga, H., 577, 596 Hulpieu, H. R., 117, 139 Hungate, R. E., 404, 416 Hunninen, A. V., 393, 400 Husnot, P., 488, 491 Hutchinson, C. M., 670, 680 Hutchinson, H. B., 9, 19 Hutner, S. H., 108, 139, 884, 902

Huxley, J., 541 Huygens, 11 Hyman, Libbie H., 304, 308, 440, 468

5,

17,

124,

139,

Ibara, Y., 175, 176, 219 Ikeda, I., 576, 661, 665 Illing, Margaret A., 496, 504

AUTHOR INDEX
Kitchen,
S.

911
F.,

Kahl, A., 59, 73, 75, 688, 690, 706,

708, 736, 804, 848, 868, 710, 740, 812, 850,

712, 742, 814, 856,

714, 762, 827, 857,

717, 767, 829, 858,

721, 728, 772, 803, 831, 847,

605, 606, 607, 608, 609, 610, 611, 627, 630 Kitching, J. A., 102, 118, 119, 120

861,863,

140 Klebs, G., 21, 37, 250 Klein, B. M., 56, 57, 66, 68, 93, 107,
740, 898, 903 Kleinschmidt, A., 54, 94

878

Kahler, H., 135, 139

Kaleita, E., 466 Kalmus, H., 117

Kamm,
567

Minnie W., 541, 542, 545

Kamptner, E., 267, 270 Kar, A., 586, 595 J. S., 434 Kartchner, J. A., 596 Kater, J. M., 176, 218 Katzin, L. I., 404, 416 Kay, M. M., 169, 218 Kay, Marie W., 693, 699 Kean, B. H., 640, 641 Keen, Jean, 311, 331 Keidel, H. J. W., 54, 94
Railing,

Kloss, H., 14, 18 Kliiver, Cessa, 612, 633 Klug, G., 334, 338, 371, 396, 400 Koch, Dorothy A., 456, 468 Koehler, O., 132, 140 Kolliker, R. A. v., 14, 18

Konig, A., 787

Koster, W., 744, 755 Koffman, M., 175, 178, 219

Kofoid, C. A., 45, 55, 66, 76, 77, 93, 108, 134, 140, 141, 154, 157, 167
219, 291, 312, 316, 327, 374, 377, 379, 390, 393, 416, 468, 776, 787, 788, 818, 819, 821, 822, 826, 845, 852, 861 Kohler, A., 132, 669, 680 Koidzumi, M., 379, 401, 404, 414, 416 Kolkwitz, R., 23, 37 Koltzoff, N. K., 61, 94 Komada, K., 101, 143, 813 Komp, W. H. W., 606, 630 Konsuloff, S., 684, 685, 689 Kopac, M. J., 104, 106, 139 Korotoneff, A., 681 Korschelt, E., 219 Korshikov, A. A., 262 Kotlan, A., 377, 401 Kozloff, E. N., 357, 366, 388, 760, 772, 778, 780, 782, 784, Kraneveld, F. C., 54, 94
168, 331, 401, 817, 841,

329
395, 816, 828,

Keilin, D., 541, 567, 678, 679,

699

...
680

Keller, H., 468 Kent, W. S., 269, 688, 736, 845, 854 858, 861, 877, 878 Kellicott, D. S., 771, 854 Kepner, W. A., 139 Kessel, J. F., 451 Kessler, W. R., 467 Ketchum, B. H. r 311, 331 Keysselitz, G., 168, 648, 659, 665 Khainsky, A., 103, 139 Kidder, G. W., 26, 37, 63, 66, 76 83, 93, 97, 101, 104, 106, 109, 136, 139, 140, 150, 152, 164, 169, 176, 210, 214, 218, 227, 244, 374, 691 699, 702, 721, 733, 736, 754, 755, 756, 760, 761, 762, 766, 772, 774 776, 777, 787, 810, 812, 884, 902
'

406

401,

788

Kikuth, W., 630

Kilborne, F. L., 14, 19, 633 Kimball, R. F., 146, 153, 193, 194
196, 219, 228, 230, 234, 235, 238

244, 839
G., 377, 400 E., 117, 142 Kinder, E., 54, 94 King, R. L., 84, 93 King, S. D., 79 King, W. V., 606, 630 Kingsbury, B. F., 82 Kirby, H. Jr., 35, 37, 71, 78, 93, 101,

Kimura, G. Kimura, T.

Krascheninnikow, S., 736 Kremp, A., 678, 679 Krichenbauer, H., 297, 308 Krijgsman, B. J., 127, 140, 360, 395, 402 Kriiger, F., 71, 73, 76, 94, 758, 773 Krukenberg, W., 106 Kruse, W., 630 Kruszynski, J., 743, 755 Kuczynski, M. H., 167, 385, 401 Kudo, R. R., 8, 9, 11, 18, 32, 35, 37,
>
>

>

140, 157, 167, 371, 377, 379, 388, 389, 391, 416, 444, 445, 736, 742, 755, 894, 902 Kirkegaard, D., 862

107, 369, 385, 412, 731, 812,

168, 381, 397, 468, 800,

363, 383, 400, 715, 807,

366,

384 404
72l' 81o'

82, 94, 99, 121, 133, 140, 163, 167, 168, 170, 176, 366, 407, 408, 416, 442, 445, 462, 468, 656, 658, 659, 660, 670, 671, 672, 674, 721, 798, 804, 812 Kudrjewzew, W. A., 903 Kuenen, W. A., 450, 469 Kiihn, A., 168, 178, 181, 219, 425 Kuhne, W., 22, 37 Kunstler, J., 71, 369

42, 46, 62, 146, 150, 179, 219, 437, 440, 649, 651, 665, 666, 676, 681,

353, 441, 655, 669, 710,

912
Kunze, W., 168 Kupper, W. H., 608, Kylin, H., 90, 94
Labb6, 681
Lackey,
6"

PROTOZOOLOGY
Lips, M., 614, 634 List, T., 223, 244 Lister, A., 434, 494 Lloyd, F. E., 119, 140, 420, 425 Loefer, J. B., 25, 26, 37, 280, 291, 304, 309, 744, 756

A.,

545, 553, 557, 558, 565,

J., 12, 16 B., 23, 37, 166, 258, 261,

Lachmann,
J.

262, 270, 304, 306, 308, 343, 344, 366, 755, 829, 831 P., 176, 216, 887, 902 Laird, JVL, 353, 366, 617, 618, 630 Lamarck, C. d., 11

Laidlaw, P.

Lambert, S. W., 641 Lambl, W., 401 Lamy, L., 797, 812 Landau, Helen, 560, 567 Landis, E. M., 153, 219 Langmuir, A. D., 607, 626 Lankester, E. R., 45 Lapage, G., 101, 140, 366, 440, 469, 579, 596
Lauterborn, R., 23, 37 Larson, Enid, 748, 755 Laveran, A., 14, 18, 228, 351, 353, 366, 622, 630 Lavier, G., 395, 401 Lawrie, N. R., 106 Lebour, Marie V., 331 Leegaard, C, 706, 721

Lohner, L., 116 Losch, F., 14, 18, 449 Looper, J. B., 30, 38, 464, 470, 507 Louttit, M., 226, 245 L0vtrup, S., 104, 106, 120, 139, 140 Lucas, Catherine L. T., 445, 459, 462, 469 Lucas, Miriam S., 63, 752, 756, 800, 812 Luce, R. H., 121, 140 Lucet, 622, 630 Ludwig, F. W., 592, 597 Lund, Barbara, 117, 140 Lund, E. E., 63, 66, 67, 94, 577, 597 832, 845 Lund. E. J., 170, 219 Luntz, A., 134, 136, 138, 140, 290, 291 Lutz, A., 666 Lutz, F. E., 38, 903 Luyet, B. J., 22, 38 Lwoff, A., 5, 18, 34, 56, 66, 74, 92,

106, 109, 112, 140, 213, 215, 219, 253, 754, 774, 776, 781, 782, 783, 784, 785, 786, 787, 789, 795
97,

Leeuwenhoek, A.
Leger, 555, 596, 676, Leger, Leidy, 416,

v., 10, 11, 13 L., 168, 252, 543, 544, 554, 557, 562, 567, 570, 575, 584, 654, 658, 666, 669, 670, 672,

Lwoff, M., 56, 92

681 M., 620, 622

J.,

Lynch, J., 740, 756 Lynch, J. E., 63, 66, 70, 94, 852 Lynch, K. M., 373, 401, 456 Lynch, R. S., 218, 244, 246

12, 18, 357, 366, 401, 412, 425, 437, 445, 469, 491, 515,

M
MacArthur, W. P., 34 MacBride, T. H., 429, 434 MacCallum, W. G., 14, 18 MacDougall, Mary S., 133,
169, 206,

567
Leiner, M., 106, 140

Leishman, W.
Lepsi,
J.,

B., 15, 18 E., 309, 338, 366 843, 845 Leuchtenberger, Cecilie 43, 95 Leuckart, G. F. R., 14, 18, LeVeque, J. A., 754, 756 Levine, N. D., 388, 401, 577, 580, 583, 596, 799, 812 Levinsohn, L. B., 62, 95, 104, 143 Lewert, R. M., 617, 630 Lewis, T. R., 14, 18 Lieberkuhn, N., 60 Lieberman, P. R., 742, 756 Liebmann, H., 168, 219, 586, 596 Liesche, W., 168, 219, 437, 469 Light, S. F., 167, 383, 401, 404, 410, 412, 416 Lillie, F. R., 213 Lilly, D. M., 109, 140, 772 Lin, C. C, 451, 452 Lindemann, E., 314, 318, 331

Lemmermann,

229, 610, 630, 731, 733, 736 Macfie, J. W. S., 452, 600, 634

Machado, A., 597 MacKinlay, Rose B., 490, 491, 543 Mackinnon, Doris L., 457, 469, 552,
563, 564, 567, 568, 572, 597

MacLennan, R.
94,

Linnaeus,

G,

11,

18

F., 63, 70, 80, 82, 85, 113, 119, 140, 150, 176, 219, 412, 416, 694, 699, 710, 721, 788, 817, 818, 819, 821, 822, 828, 861 MacNeal, W. J., 15, 19, 351, 367, 631, 886 Maegraith, B., 33, 38, 605, 630 Magath, T. B., 586, 597 Mainx, F., 53, 94, 285, 291, 293, 294, 309 Malmsten, P. H., 14 Manceaux, L., 625, 631 Manifold, J. A., 639 Manresa, M. Jr., 579, 595 Mantz, F. A., Jr., 626, 631

AUTHOR INDEX
Manwell, R. D., 169, 219, 605, 608, 615, 617, 625, 631, 633, 838, 845 Marshall, E. K., 597 Marsland, D. A., 891, 902 Marsson, M., 23, 37 Martiis, L. C. de, 567
Martin, C. H., 401 Martin, G. H., 429, 434 Martin, G. W., 312, 320, 326, 331 Martini, E., 212 Mast, S. O., 26, 46, 52, 75, 82, 83,
84, 91, 94, 101, 105, 107, 109, 112, 121, 124, 126, 130, 133, 140, 141, 175, 176, 178, 219, 274, 275, 291, 294, 437, 440, 441, 469, 852, 861,

913

Milovidov, P. F., 433 Minchin, E. A., 40, 55, 253, 367 Missiroli, A., 671, 682 Mitchell, W. H., 177, 216 Miyashita, Y., 699, 788, 794, 795

Mjassnikowa, Marie, 788

Moewus,

F., 167, 181, 207, 223, 229, 231, 245, 277, 291

Mohan, B. N., 617, 632 Mohr, J. L., 754, 756, 847, 848
Molisch, H., 22, 38

882 Mathis, C, 620, 622 Matsubayashi, H., 585, 597 Mattes, 6., 893, 902 Matthews, C. B., 610, 627

Maupas, E.

F.,

13,

187,

190,

193,

199, 202, 209, 219,

Maurer, G., 605, 631 Mavor, J. W., 357, 367, 649, 666

May, G.
Mayne,

H., 135, 137

L., 582, B., 608, 631

Mayer, M., 631

Moore, Emmeline, 393, 401 Moore, E. N., 597 Moore, Imogene, 79, 209, 803, 812 Morea, L., 26, 27 Morehouse, N. F., 337, 338 Morgan, B. B., 388, 401 Morgan, T. H., 213 Morgenthaler, O., 670, 682 Moroff, T., 597 Morris, S., 445, 469 Moses, M. J., 44, 94 Most, H., 97, 141 Mouton, H., 106, 141, 175, 220 Mowry, Helen A., 817, 828 Moynihan, I. W., 582, 597

Mayhew, R.

597

Mudrow,
Mueller,

Lilly, 615, 631 Miihl, Dorothea, 528, 544, 568

Mazia, D., 133, 141 McBride, E. W., 82

D., 63, 799, 812 McGann, Virginia G., 244 McKay, F., 337, 338 McKibben, W. R., 297, 308 McLennan, E. I., 423, 425 McNeal, Ethel, 373, 393, 401 Meglitsch, P. A., 445, 469, 649, 655, 656, 666, 798 Mehlman, B., 886, 903 Meldrum, N. U., 118, 141 Meleney, H. E., 226, 243, 244, 448, 450, 452, 453, 470, 888 Mercado, Teresa I., 614, 631 Mercier, L., 168, 187, 444, 469, 546,
J.

Miiller, J., 12,

J. F.,

517
859, 861

McDonald,

Miiller, O. F., 11, 13 Miiller, W., 191, 220, 744,

756

Mugard, Helene, 763, 769, 772, 795,

860, 861 Mulligan, H. W., 605, 613, 614, 631, 633

Mulsow, K., 207, 220, 532, 568 Mulsow, W., 169 Murer, H. K., 412, 416 Musacchia, X. J., 442, 469
Musfeldt, I. W., 640, 641 Musgrave, A. J., 563, 568 Musgrave, W. E., 15, 18 Mutafowa, R., 820, 826, 883 Myers, E. H., 168, 494, 496, 504

568

Merriman, D., 837, 845 Merton, H., 132, 141

Mesnil, F., 351, 353, 366, 591, 641,

N
Nabih, A., 590, 597 Nageli, K. W., 682 Nagler, K., 443
Nasset, Elizabeth C., 134, 141

663
Metalnikoff,
S., 103, 141 S., 209, 220 Metcalf, M. M., 8, 18, 168, 684, 685, 686, 689 Metchnikoff, E., 102, 141 Metz, C. B., 197, 200

Metalnikov,

Nassonov, D., 78, 79, 85, 94 Nauss, Ruth N., 424, 425
Naville, A., 157, 168, 187, 208, 220, 563, 565, 568, 573, 590, 597, 646, 649/655, 656, 657, 666 Needham, J. G., 23, 38, 881, 903 Negri, A., 641 Neiva, A., 812 Nelson/E. C, 799, 812, 826, 828, 889, 890 Nelson, R., 367 Nemeczek, A., 649, 666, 890
|

Meyer,

699 Michaelis, G., 238, 244 Michaelis, P., 238, 244 Michelson, E., 745, 746 Milam, D. F., 614, 631 Miller, E. d. W., 136, 141 Miller, F. W., 388, 397 Miller, W. W., 597
S. L., 114,

914
Nenninger,

PROTOZOOLOGY
Patterson, E. K., 106, 137 Patton, W. H., 631 Paul, J. H., 606, 632
Pavillard,
J.,

Ursula, 850, 852, 853, 854, 856, 857, 862 Neresheimer, E., 52, 61 Nicolle, C, 625, 631, 886 Nie, D., 364, 367, 373, 374, 377, 402, 457, 461, 469, 752, 756, 799, 812 Nieschulz, O., 350, 367, 395, 402, 457,

292

Pearson, N. E., 710, 721

Pelaez, D., 618, 632

Penard, E., 71, 75, 87, 95, 212, 425,

437, 440, 470, 477, 491, 506, 515, 713, 722, 724, 736, 862 Penfold, W. J., 451 Penn, A. B. K., 169, 190, 220, 838,

469
Nigrelli,

R.

F., 80, 92, 321, 331,

372

402, 655, 666

Niimi, D., 337, 338 Nirenstein, E., 103, 104, 141 Noble, A. E., 852 Noble, E. R., 168, 220, 457,

846 Pennypacker, M.
469,

I.,

390, 402

533, 568, 649, 650, 651, 666 Noble, G. A., 457, 469 Noller, W., 350, 366, 579, 588, 597, 618, 631 Noland, L. E., 27, 38, 116, 141, 200, 220, 388, 401, 701, 705, 706, 712, 713, 717, 721, 725, 728, 736, 767, 769, 771, 773, 800, 812, 841, 846 855, 862 Novy, F. G., 15, 19, 351, 367, 631, 886 Nozawa, T., 585, 597 Nyholm, K.-G., 423, 425

Perard, C, 577, 597, 735 Perez, C, 676, 682 Perty, J. A. M., 12, 19, 477 Perzewa, T. A., 691, 699 Peschkowsky, Ludmilla, 797, 812
Pestel, B., 867, 878 Peters, N., 312, 331 Petersen, J. B., 53, 95,

O'Connor, F. W., 373, 450, 451, 452 Oehler, R., 176, 220 Ohmori, J., 680 Oshima, K., 670, 682 Okada, Y. K., 441, 469, 508, 515 Opitz, Pauline, 194, 195, 218 Ordal, E. J., 419, 426 O'Roke, E. C, 620, 631 Owen, H. M., 95, 256, 270, 343
Pace, D. M., 26, 112, 117, 141, 274, 275, 883 Pack, A., 712 Packchanian, A., 349, 367 Paillot, A., 674, 682

256 Petruschewsky, G. K., 649, 666 Phelps, A., 27, 38, 112, 743 Phelps, Lillian A., 213 Phleger, F. B., 496, 504 Pickard, Edith A., 63, 95, 142, 779, 788 Piekarski, G, 55, 95, 228, 245 Pierson, Bernice F., 147, 839, 841, 846 Pig6n, A., 120 Piney, A., 82, 95 Pinto, C, 541, 544, 568, 649, 666
Pitelka,

Dorothy
I.,

R., 53, 54, 95, 304,

309
312, 331 Pochmann, A., 297, 309 Pohl, A. W., 121, 140 Poisson, R., 306, 309, 557, 568, 678,
Playfair, G.

682
Poljansky, G., 693, 797, 812, 817
J. I., 699 W., 43, 95 M., 169, 206, 228 P. P., 903 Annie, 664, 671, 672, 680 R. J., 602, 632 Posey, F. M., 640, 641 Post, Rita J., 496, 504 Powell, W. N., 166, 379, 402 Powers, E. L., 220, 228, 235, 245 Powers, J. H., 287, 292 Powers, P. B. A., 107, 142, 168, 706,

Poljanskij,

Pollister, A.

Palm, B.

T., 433,

434

Palmer, T. C, 299, 309 Pantin, C. F. A., 124, 142 Panzer, T., 114, 142 Parducz, B., 767, 769, 773
Parisi, B., 649, 666 Park, O., 79, 95 Parker, F. L., 496,

Popoff, Popoff, Porter, Porter,

504

Parker, R. C, 744, 756 Parks, R. E., Jr. 884, 902 Pascher, A., 167, 181, 250, 252, 253
257, 258, 259, 267, 270, 272, 275, 277, 281, 288, 291, 294, 299, 303, 309, 314, 331, 335, 338, 341, 342,

722, 741, 749, 750, 756, 762, 769, 773, 800, 812

Prandtl, H., 168, 206, 220, 705, 722

Prashad, B., 667

Pratje, A., 114, 142, 318, 331 Pratt, H. D., 349, 368 Pratt, I., 597 Precht, H., 850, 862 Preer, J. R. Jr., 239, 240, 241, 245 Prehn, Marianne, 649, 667

367
Pasteur, L., 14, 19, 670, 682 Patten, M. W., 153, 220 Patten, R., 168, 574, 597 Patten, Ruth, 684

AUTHOR INDEX
Prescott, G. W., 312, 331 Pringsheim, E. G., 90, 95, 97, 108, 109, 142, 181, 185, 250, 253, 277, 283, 292, 293, 294, 297, 299, 303, 304, 309, 744, 756, 884, 903 Proske, H. O., 605, 627 Prosser, C. L., 126, 141 Provasoli, L., 108, 139, 884, 902 Prowazek, S. v., 169, 744 Pruthi, H. S., 27 Prytherch, H. F., 560, 568 Putter, A., 116, 142 Purkinje, J. E., 12 Putnam, P., 605, 610, 630 Puytorac, P. de, 70, 95, 691, 697, 699

915

Rimington, C, 605, 632 Rita, G., 586, 598 Robertson, A., 584, 598 Robertson, Muriel, 367, 401 Robertson, T. B., 110, 111, 112, 142 Rodhain, J., 459, 470 Romanowa, K., 355, 367 Root, F. M., 225, 245, 450, 452, 470, 868, 873, 878 Rose, Elizabeth K., 626, 633 Rose, M., 415 Rosenberg, L. E., 38, 175, 178, 220, 390, 402, 852, 861, 862 Rosenhof, R. v., 11, 19 Roskin, G., 51, 60, 61, 62, 95, 99, 104,
143, 351, 355, 367, 420, 425, 506,

515

Quinby, G.

E., 607,

626

Ross, R., 15, 19, 608, 632

Raabe, H., 148, 165, 220, 440, 470, 836, 846 Raabe, Z., 699, 774, 776, 779, 783, 787, 788 Rafalko, J. S., 168, 220, 436, 470 Raffaele, G., 602, 632 Raffel, D., 218, 244 Rakoff, A. E., 402 Rampi, L., 312, 331, 816, 828 Ramsey, Juanita, 682 Raper, K. B., 433, 434 Ratcliffe, H. L., 459, 467, 470, 632, 799, 887, 903 Ray, Dixie L.,'98, 142 Ray, H. N., 469, 543, 552, 563, 564
Redi, F., 11 Rees, C. W., 63, 388, 398, 402, 624,
632, 735 Regendanz, Reichenow,
145, 321, 588, 625, 146, 331, 590, 631,
P., 624, 632 E., 45, 90, 95,

Rossenbeck, H., 898, 902 Rossolimo, L. L., 691, 699, 773 Roubaud, E., 452

Roudabush, R.

L., 351, 367, 579, 583, 592, 598, 618, 620, 628

Roudsky, D., 228 Routh, C. F., 586, 594 Roux, H., 799, 812 Roux, J., 722, 846 Rudzinska, Maria A., 870, 878 Rumjantzew, A., 45, 51, 95, 112,

143,

508, 515 Russel, E. J., 19 Russell, P. F., 605, 606, 608, 617, 632,

633

115, 177, 220, 253, 277, 425, 459, 466, 565, 594, 597, 598, 615, 632, 688, 826, 828 Reinhardt, J. F., 579, 598 Renn, C. E., 418, 425 Reuling, F., 387, 402 Reyer, W., 893, 903 Reyes, R. P., 618, 632

142, 292, 568, 624,

Reynaerts-De Pont, F., 117 Reynolds, B. D., 30, 34, 38, 168, 225,
245, 341, 360, 367, 464, 465, 470, 747, 756 Reynolds, Mary E. C, 153, 220, 832, 846

Sabin, A. B., 626, 633 Sahrhage, H., 808, 812 Sailey, H. R., 626, 631 Samuels, R., 167, 390, 402 Sanders, Elizabeth P., 16, 92, 216, 226, 243, 398, 415, 447, 459, 467, 470, 888, 902 Sandon, H., 28, 38 Sandza, J. G., 888, 901 Sanford, Mary F., 404, 416 Santos-Pinto, J. d., 327, 331 Sapiro, J. J., 226, 245 Sassuchin, D. N., 115, 143, 894, Sauerbrey, Ernestine, 725, 736,

137, 458,

903
843,

846 Saunders, E. R., 102, 138 Saunders, J. T., 75, 95

Schaeffer, A. A., 114, 121, 124, 143, 437, 440, 442, 470 Schaudinn, F., 13, 15, 19, 99, 105, 155, 470, 526, 566, 598, 600, 605

Rhodes, R. G, 371 Rhumbler, L., 97, 105, 122, 123, 133, 142, 220, 504 Rice, N. E., 440, 470 Rice, V. J., 649, 667 Richards, O. W., 112, 142 Richardson, K. C, 82, 95 Richardson, L. R., 664, 672, 680

633
Schellack,

C,

588, 590, 598

Scherffel, A., 250, 253, 257, 271, 360,

367
Schewiakoff, W., 120, 143, 767 Schiffmann, Olga, 544, 568

916

PROTOZOOLOGY
Smith, Th., 14, 19, 336, 338, 591, 598, 633 Snyder, T. L., 447, 450, 470 Sokoloff, B., 213, 220 Sonneborn, T. M., 7, 19, 146, 151,
153, 169, 190, 191, 192, 193, 196, 206, 218, 221, 229, 233, 236, 237, 238, 239, 241, 242, 243, 245 Soule, M. H., 117, 143

Schiller, J., 257, 258, 267, 271, 281,

292, 312, 316, 318, 320, 324, 328,

331
Schilling, A., 331

Schindera, M., 357, 367 Schischliaiewa, S., 351, 367

Schmahl, O., 175, 221, 797, 798, 813 Schmidt, W., 53, 393, 402 Schneider, A., 545, 557, 568, 598 Schneider, H., 212, 326, 332 Schoenborn, H. W., 26, 38, 302, 309 Schrader, F., 672, 682 Schroder, B., 223, 245 Schroder, O., 61, 95, 667, 682 Schuberg, A., 62, 95, 682, 818 Schubotz, H., 121 Schiiffner, W., 605, 633 Schussler, H., 303, 309 Schulz, J. A., 136, 817, 826 Schulze, B., 277, 280, 288, 289, 292 Schulze, K. L., 143 Schumacher, J., 115 Schumaker, E., 364, 366 Schussnig, B., 420, 425 Schwartz, V., 213, 806, 813 Schwarz, G. A., 626, 633 Scott, J. W., 640, 641 Scott, Miriam J., 799, 813
Scremin, L., 55, 91 Seaman, G. R., 106, 143 Seguela, Josephine, 844, 845 Sergent, Ed., 600, 615, 633 Sergent, Et., 600, 633 Setna, S. B., 566 Seyd, E. L., 803, 813 Shannon, R. C, 606 Shapiro, N. N., 103, 143 Sharp, R., 63, 95, 816, 822 Shaw, W. R., 292 Shawhan, Fae M., 303, 309 Sheather, L., 579 Shortt, H. E., 355, 367, 602, 603, 633 Shumway, W., 323, 332 Siebold, C. T. E. v., 12, 19 Siedlecki, M., 15, 19 Sikama, Y., 710, 722 Silva Estela de S. E., 816, 828 Silverstein, J. K, 467 Simmons, J. S., 633 Simon, C. E., 393, 395, 402
Singh, B. N., 25, 38, 176, 178, 221, 303, 308, 423, 426, 433, 434, 436, 437, 443, 470 Sinton, J. A., 607, 633 Skogsberg, T., 328, 332 Skvortzow, B. W., 277, 292, 297, 299,

Southwell, T., 667 Specht, H., 117, 143 Spector, B. K, 226, 449, 467 Speeth, Caroline, 508, 515 Spencer, H., 71, 209, 222, 700, 722
Spiegel, A., 806, 813 Spindler, L. A., 639, 641 Spingarn, C. L., 889, 903 Sprague, V., 168, 208, 221, 529, 568, 638, 641, 656, 666, 682 Sprugel, G., Jr., 28, 38, 806, 813 St. Remy, G., 639, 641 Stabler, R. M., 167, 168, 227, 387, 388, 390, 402, 456, 457, 467, 470 Stammer, H.-J., 854, 862 Starcovici, C, 633 Stein, F., 12, 14, 19, 202, 221, 688, 736, 846 Steinecke, F., 90 Stempell, W., 32, 38, 120, 143, 672, 682 Stern, C, 26, 156, 511, 515 Steuer, A., 324, 332 Stevens, N. M., 788, 811, 813 Stiles, C. W., 722 Stiller, J., 850, 862 Stokes, A. C, 12, 19, 271, 309, 722, 736, 846, 852, 862 Stole, A., 105, 106, 143, 212

544,

246, 459,

270,

670,

688,

Stolkowski,
Stolte,

J.,

721

H. A., 176, 221, 804, 806, 813 Stowell, R. E., 898, 903 Stranghoner, E., 744, 756

Stratman-Thomas, W.
608, 609, 627, 633

K,

602, 607,

Strelkow, A., 70, 96, 817, 824, 828 Strickland, A. G., 222, 747, 756 Strong, R. R, 799, 813
Stuart, C. A., 176, 218, 221, 244, 756 Stuckey, R. G., 107, 136, 706, 720 Studitsky, A. N., 779, 788 Stump, A. B., 168, 485, 492 Summers, F. M., 136, 148, 213, 215, 218, 221, 691, 699, 733, 736, 839, 843, 845, 846, 857, 862 Sutherland, J. L., 371, 402, 406, 416 Swaminath, C. S., 355, 367 Swarczewsky, B., 635, 641, 847, 849, 857, 859, 862, 867, 870, 875, 878 Swellengrebel, N. H., 450, 469 Swezey, W. W., 63, 826, 828 Swezy, Olive, 45, 55, 76, 77, 94, 108, 140, 154, 157, 167, 168, 219, 221, 312, 374, 416

309
Slane, Gertrude M., 134, 144 Smith, L., 579, 595 Smith, L. M., 545, 568 Smith, G. M., 271, 282, 285, 292 Smith, Nanine M., 458, 466, 886

AUTHOR INDEX
Swirenko, 290, 292 Szab6, M., 828

917

U
Uhlhorn, E., 577, 598 Ujihara, K., 226, 246 Uribe, C, 168 Usinger, R. L., 349, 368 Uyemura, M., 21, 38, 774, 777, 788, 800, 813

Taft, C. E., 288, 292 Tai, L.-S., 328, 332 Talbott, Mary, 818, 822, 826 Taliaferro, Lucy G., 351, 368, 612, 614, 633 Taliaferro, W. H., 33, 38, 226, 246, 351, 367, 368, 470, 605, 612, 613, 614, 615, 628, 633 Tanabe, M., 101, 143, 167, 375, 398, 586, 598, 813 Tartar, V., 194, 221 Tate, P., 463, 466, 602, 615, 626, 630 Tavolga, W. N., 372, 402 Taylor, C. V., 57, 63, 65, 70, 96, 129, 143, 175, 178, 213, 222, 747, 756, 884, 903

Valentin, 14, 19 Valkanov, A., 426, 473, 492, 506, 513,

515

Van Overbeek de Meyer,

685, 689

G. A. W.,
238, 246,

Van Wagtendonk, W.
884, 903

J.,

Vasudevan,

A.,
J.,

639
107, 143

Veley, Lilian

Teichmann,

E.,

641

Tejera, E., 453 ten Kate, C. G. B., 62, 68, 96, 686, 689, 705, 710, 722, 804, 806, 813

Verworn, M., 39, 52, 96, 98, 127, 133, 135, 143, 212 Vevers, H. G., 32, 38 Vianna, G., 368 Vickers, Marjorie A., 622, 629
Vincent, Mary, 547, 557, 569, 592,

Terby,

J., 168 Terzian, L. A., 617, 633 J., 113, 138, 856, 861 Theiler, H., 390, 402 Thelohan, P., 584, 598, 649, 667 Thimann, K. V., 178, 222 Thompson, P. E., 602, 617, 618, 633 Thompson, R. H., 312, 313, 314, 318,

598
Vida, B. L. D., 586, 598 Vincke, I. H., 614, 634 Visscher, J. P., 63, 73, 96 Vlk, W., 53, 96, 256 Voegtlin, C, 135, 139 Volk, J., 577, 585, 595 Volkonsky, M., 443, 470

Thaureaux,

320 332

Thompson, Sally, 862 Thomson, D., 450 Thomson, J. G., 367,

605, 634

von Brand,
450, 584, 598,

Volz, P., 472, 492 T., 175, 178, 222, 839, 846, 856, 862, 886, 903

Thon, K., 96, 153, 222, 704, 722 Thorpe, Mary V., 615, 626
Threlkeld, W. L., 168, 465, 470 Tiffany, L. H., 290, 292 Tobie, Eleanor, J., 96, 886, 903 Tonniges, C, 74, 96
Toit, P. J. d., 622, 634 Trager, W., 106, 143, 391, 402, 617, 634, 885, 889, 903

W
Wailes, G. H., 312, 329, 332, 491, 506, 515, 865, 867, 878 Walker, E. L., 471, 883 Wallengren, H., 776, 788, 846, 847, 849, 859, 862 Walton, W. R., 496, 504 Wampler, F. J., 615, 634

Ward, H.

Travassos,

L.,

812

Travis, B. V., 374, 377, 388, 395, 402, 548, 566

Treillard, M., 34

Trembley, A., 11, 19 Troisi, R. L., 533, 534, 568

Troitzkaja, O. V., 265, 271 Trussell, R. E., 386, 387, 402, 885,

902 Tsuchiya, H., 395, 403, 582, 594 Turner, J. P., 66, 81, 96, 114, 143,
147, 169, 222, 747, 756, 837, 841,

B., 667 Warner, Kay L., 104, 139 Warren, A. J., 602, 634 Waters, P. C, 395, 403 Watson, Minnie, 528, 529, 541, 544, 545, 550, 552, 554, 555, 557, 569 Watson, S. W., 418, 419, 426 Weatherby, J. H., 87, 96, 120, 143 Weineck, E., 105, 144 Weiner, Eleanor, 35 Weinman, D., 626, 634 Weinstein, P. P., 349, 368 Weiser, J., 670, 682 Weismann, A., 13, 208

846 Tyzzer, E. E., 337, 338, 453, 462,

470, 580, 581, 582, 583, 587, 588,

598

Weissenberg, R., 375, 403, 641, 672, 682 Weisz, P. B., 45, 46, 81, 96, 148, 202 213, 222, 804, 806, 813

918

PROTOZOOLOGY
371, 403, 703, 744, 385, 457, 708, 756,

Wenrich, D. H., 35, 167, 168, 222,

337, 338, 363, 368, 388, 389, 390, 398, 462, 463, 467, 471, 723, 727, 736, 742, 773, 894, 903 Wenyon, C. M., 230, 246, 368, 373, 390, 403, 450, 471, 566, 598, 634, 903 302, 387, 460, 722, 767,

351, 353, 451, 452,

Wolfson, 22, 38 Wolfson, Fruma, 613, 615, 617, 625, 629, 634 Wood, Fae D., 349, 351, 368 Wood, S. F., 349, 368, 615, 634 Woodcock, H. M., 55, 96, 451 Woodcock, A. H., 312 Woodhead, A. E., 699 Woodruff, L. L., 11, 19, 71, 96, 151,
153, 154, 190, 196, 197, 209, 214, 222, 700, 722, 744, 757, 813

Werbitzki, F., 228

Wermel, E. W.,

26, 45, 51, 95, 112, 143, 464, 471, 508, 694, 699 Weschenfelder, R., 168, 208, 222, 555,

Wrisberg, H. A., 11, 19 Wu, H. F., 686, 689

560 Wesenberg-Lund, C, 223, 246 West, E., 629 West, G. S., 271, 275, 292 West, L. S., 608, 615, 633 Wetzel, 96, 512, 515, 685, 689 Weyer, G, 839, 846 Whedon, W. F., 327, 332 Whipple, G. C, 114, 144 White, G. F., 670, 682 Whitlock, W. C, 139

Yamasaki, S., 353, 368 Yarborough, N., 15, 16, 889 Yocom, H. B., 25, 38, 63, 65,
Yonge, Yorke, 887 Young, Young, Young,

96, 118, 144, 169 C. M., 108 W., 450, 451, 471, 600, 634,

Wichterman,

R., 144, 190, 199, 742, 744, 756, 843, 846, 884,

26, 27, 38, 121, 134,

Dixie, 804, 813 E. L., 418, 419, 426 M. D., 608, 628, 631

204, 222, 393, 400, 804, 806, 812, 813,

903

Wickware, A.

B., 620,

634

Wilber, C. G., 82, 96, 106, 107, 123, 134, 144, 440, 442, 471 Williams, G. W., 697, 699 Willis, A. G., 649, 655, 667 Wilson, E. B., 151, 222 Wilson, H. V., 442, 471 Winger, R. N., 577, 596 Winter, Mary W., 613, 634 Wohlfarth-Bottermann, K.-E., 73, 75, 96 Wolcott, G. B., 351, 368 Wolff, E., 222

Zander, E., 670, 671, 682 Zeliff, C. C, 379, 403 Zeuthen, E., 116, 144 Zill, L. P., 238, 246 Zimmerman, H. E., Jr., 639, 641 Zingher, J. A., 114, 144 Zopf, W., 426 Zuckerman, Lucille K., 226, 244 Zublin, E., 598 Zuelzer, M., 45, 118, 134, 144 Zulueta, A. de, 62 Zumstein, H., 109, 144, 250, 253 Zweibaum, J., 82 Zwetkow, W. N.. 569

Subject Index
in bold-face type indicate pages on which are given the definitions, explanations, or discussions of technical terms; the characterizations or differentiations of taxonomic subdivisions; or the descriptions of genera and species. Numbers in italics indicate pages on which appear those illustrations that

Numbers

could not be placed on the same pages as the related text matter.
Actinobolina, 707
Abiogenesis, 11
borax,

707-708

Abnormal morphology, 109-110, 111 Acanthamoeba, 443

castellanii, 441, 443 hyalina, 24, 441, 443 Acanthociasma, 519 planum, 520 Acanthociasmidae, 519 Acanthocystidae, 506, 511-513

Actinobolinidae, 700, 707-708 Actinobolus, 707 Actinocephalidae, 541, 554-558 Actinocephalus, 554-555 acutispora, 558, 555 parvus, 555

Acanthocystis, 25, 511

aculeata, 26, 155, 511,

512
867
867, 868

Actinocoma, 506 ramosa, 506, 507 Actinocomidae, 506 Actinolophus, 510

pedunculatus, 509, 510 Actinomonas, 335 mirabilis, 335, 336 Actinomyxidia, 76, 643, 660-663 Actinophryidae, 506, 507-508 Actinophrys, 22, 507, 883 sol, 205, 507 vesiculata, 508 Actinopoda, 417, 505-524 Actinosphaerium, 11, 40, 45, 117, 508, 883 arachnoideum, 508
eichhorni, 26, 44, 51, 204, 212, 507,

Acanthodactylus vulgaris, 588

Acanthogammarus

albus,

victorii,

Acanthometridae, 519 Acanthometron, 519 elasticum, 62, 520 Acanthoma, 519 teracopa, 520 Acanthoniidae, 519 Acanthospora, 554 polymorpha, 553, 554 Acanthosporidae, 541, 554 Acartia, clausi, 324, 794 Accipiter cooperii, 586 Acephalina, 530, 531-541
Acetylcholinesterase, 106 Achlya glomerata, 434

508
Actinotricha, 822 Actinozoa, 789 Actipylea, 519-520 Acutisopora, 550-551 macrocephala, 551 Adaptability of Protozoa, 28, 34, 101 Adelea, 79, 590 ovata, 589, 590 Adeleidae, 590-592 Adeleidea, 570, 590-594 Adelina, 590
deronis, 168, 208, 590

Achromatic figure, 157, 158 Acidified methylgreen on nucleus, 42 Acilius sulcatus, 855 Acineta, 870
cuspidata, 870, 871 lacustris, 869, 870 tuberosa, 870, 871 873 Acinetaria, 863 Acinetidae, 863, 870-875 Acinetopsis, 873 tentaculata, 872, 873 Acis, 552
,

Acmaea, 859
persona, 111 Acnidosporidia, 526, 635-642
Acridin, 228 Actineliidae, 519 Actinelius, 519 primordialis, 520 Actinia equina, 789

mesembryanthemum, 789

dimidiata, 590, 591 octospora, 590, 591 Adoral membranellae, 59, 63 zone, 58, 59 Aedes, 606, 615, 617 aegypti, 530, 538, 617, 672 albopictus, 538, 617 Aegyria, 730 Aeschna constricta, 558 Aethalium septicum, 106 African Coast fever, 625

919


920
Agarella, 658 gracilis, 658, 659

PROTOZOOLOGY
Amoeba
continued
dofleini, 101

Aggregata, 79, 573

eberthi,

573-574

dubia, 52, 101, 120, 437, 438 gorgonia, 489, 440

guttula, 49,

Aggregatidae, 571, 572-576 Aging in Protozoa, 208-211

Agriodrilus, 698

438

Umicola, 438-439
meleagridis, 335 proteus, 28, 41, 49, 52, 79, 80, 82, 98, 101, 117, 119, 120, 123, 124, 125, 126, 169, 170, 212, 437, 438, 882 radiosa, 21, 49, 101, 439, 440 spumosa, 41, 49, 439-440 striata, 46, 49, 437-438 verrucosa, 21, 24, 25, 46, 98, 118, 122, 128, 437, 438 vespertilio, 439, 440 Amoebiasis, 446, 449 Amoebic dysentery, 446, 449 Amoebidae, 435, 437-443 Amoebina, 418, 435-466

Agriolimax agrestis, 34, 747 Agrion puella, 549 Aikinetocystidae, 531, 535-536 Aikinetocystis, 536 singularis, 535, 536 Akaryomastigont, 397 Albertisella, 535 crater, 535 Algae, 420, 422 Alisma, 434 Allan tocystidae, 531, 540 Allantocystis, 540 dasyhelei, 540-541 Allantosoma, 873 brevicorniger, 874, 876 dicorniger, 874, 876 intestinalis, 874, 876 Allelocatalysis, 111, 112 Allogromia, 472 Alloiozona, 720 trizona, 719, 720 Allolobophora caliginosa, 696 Allomorphina, 503 trigona, 508 Allosphaerium, 733 caudatum, 733 convexa, 733 granulosum, 733 palustris, 732, 733 sulcatum, 733 Allurus tetraedurus, 696 Aloricata, 850-857 Alouatta, 612 Alpha granules, 83 Alveolinella, 500 mello, 498 Alveolinellidae, 499 Amara augustata, 555 Amaroucium, 561 Amaurochaete, 431 fuliginosa, 431 Amaurochaetidae, 431 Ambystoma tigrinum, 688 Ameiurus albidus, 709 Amiba, 437 Amicronucleate ciliataes, 153-154, 189 Amitosis, 145-154 Ammodiscidae, 497 Ammodiscus, 497 incertus, 497 Ammonia, 120

Amoebodiastase, 106

Amoeboid movement, 122-126, 417 Amphacanthus, 818

Amphibia,
ovum-rajae, 818 14, 335, 393, 462, 583, 625, 651, 656, 723, 800, 852,
352, 374, 377, 390, 586, 588, 591, 592, 686, 687, 688, 694,

860

Amphidinium, 318 fusiforme, 318, 819 lacustre, 24, 318, 319 scissum, 318, 819 Amphileptidae, 723-725
Amphileptus, 27, 723 branchiarum, 723, 724 claparedei, 24, 723, 724 meleagris, 723 Amphilonche, 520 hydrometrica, 520 Amphilonchidae, 519

Amphimonadidae, Amphimonas, 358

339,

358-360

Amoeba,

21, 22, 34, 42, 52, 128, 131,

437, 883 biddulphiae, 118 discoides, 120, 437, 438

globosa, 358, 359 Amphimixis, 203 Amphionts, 538 Amphioxus, 758 Amphipoda, 754 Amphisiella, 833 thiophaga, 833 Amphisteginidae, 502 Amphithoe sp., 847 Amphitrema, 486 flavum, 485, 486-487 Amphiura squamata, 793 Amphizonella, 480 violacea, 480-481 Amphorocephalus, 556 amphorellus, 556 557 Amphoroides, 555 calverti, 558, 555 Ampullacula, 720 ampulla, 720
t


SUBJECT INDEX
Amyda
spinifera, 583

921

Amylase, 106 Anabolic products, 112-115 Anacanthotermes ochraceus, 407 Anal cirri, 58, 66 Anarma, 874 multiruga, 874-875 Anas domesticus, 588 p. platijrhyncus, 377, 620 rubripes tristis, 620 Anaspides tasmaniae, 541 Ancistrella, 778 choanomphali, 778 Ancistrina, 777 ovata, 775, 777 Ancistrocoma, 780 pelseneeri, 780, 781 Ancistrocomidae, 774, 780-784 Ancistrodon mokasen, 458-459 Ancistrospira, 779 veneris, 779 Ancistrum, 776 Ancistruma, 63, 776 isseli, 775, 111 japonica, 775, 111 mytili, 67, 775, 111 Ancyromonas, 344 contorta, 348, 344 Ancyrophora, 554 gracilis, 553, 554

Anopheles continued maculipennis freeborni, 606 pseudopunctipennis, 606 punctipennis, 606

quadrimaculatus, 606, 607, 617, 671
walkeri, 606 Anophrys, 750 aglycus, 749, 750 elongata, 749, 750 Anoplophrya, 691

marylandensis, 691, 692

orchestii, 691, 692 Anoplophryidae, 691-694 Antelope, 799, 820, 822 Anthophysa, 361 Anthophysis, 11, 361 vegetans, 361 Anthropoid apes, 799, 820, 826 Anthorhynchus, 555 sophiae, 556 Antibiotics, 154, 452, 889 Antigenic relationship, 227, 241-242. 243 Anurosporidium, 637 pelseneeri, 637 Aphrydium versatile, 867 Apis mellifica, 10, 459, 670 Apocynaceae, 353 Apodinium, 322-323 mycetoides, 322, 323 Apolocystis, 532 gigantea, 532-533 minuta, 582, 533 Apomotis cyanellus, 651

Anderotermone, 181 Anemonia sulcata, 789 Angeiocystis, 576 audouiniae, 576 Anguilla vulgaris, 353 Anguispira alternata, 357
Angulochrysis, 261
erratica, 262 Anisocomides, 782 zyrpheae, 782, 783 Anisogametes, 180 Anisogamy, 185, 187 Anisolobus, 546-547 dacnecola, 546, 547 Anisonema, 303

acinus, 303, 305 emarginatum, 303, 305

truncatum, 303, 305

Anisonemidae, 293, 303-306

Annelida, 321,
531, 532, 533, 534, 535, 536, 537, 543, 635, 636, 638, 661, 662, 663, 691, 694, 696, 697, 698, 779, 852

Annulus, 310 Anodonta, 769 Anomalina, 503

punctulata, 503

Apostomea, 66, 690, 789-795 Aquarius najas, 678 Arachnida, 556 Arachnula, 422 impatiens, 421, 422 Arboroid colony, 174, 342, 361 Arcella, 24, 45, 476, 883 artocrea, 477, 478 catinus, 411 dentata, 225, 477-478 discoides, 477 mitrata, 411 polypora, 225 vulgaris, 44, 45, 476-477 var. angulosa, 477 gibbosa, 477 Arcellidae, 472, 476-482 Archotermopsis wroughtoni, 410 Arctia caja, 670 Arcyria, 432
punicea, 431 Arcyriidae, 432 Arenicola ecaudata, 539 Argentophilous substance, 56, 78 Argyrome, 691, 697 Armadillos, 349 Arsenic acid, 227 Artificial digestion, 34, 42

Anomalinidae, 503 Anopheles, 7, 602, 606, 674 albimanus, 606 crucians, 606 dureni, 614 maculipennis, 671

922
Artodiscus, 473 saltans, 473, 474
Ascaris, 463 Ascartia, 693 Ascidia, 459

PROTOZOOLOGY
Aulacantha, 523 scolymantha, 523 Aulacanthidae, 523 Aulomonas, 344 purdyi, 343, 344 Aulosphaera, 523 labradoriensis, 523 Aulosphaeridae, 523

mentula, 785 Ascidians, 459, 674, 785, 845 Asclepiadaceae, 353

Ascoglena, 300
vaginicola,

Autogamy,
645

151,

191,

196, 238, 644,

300

Asellus aquaticus, 854, 867 Asexual reproduction, 175-180 Asida, 552 opaca, 552

Autoinfection, 538

Asio flammeus, 586 Askenasia, 705 faurei, 704, 705 Aspergillus, 639
Aspicularis tetraptera, 390 Aspidisca, 24, 845 lynceus, 148, 149, 842, 845 polystyla, 842, 845 Aspidiscidae, 832, 845

Automixis, 203-206 Autotrophic nutrition, 107-108 Averintzia, 486 cyclostoma, 486

Avian Plasmodium, 614-617

Axial
fibrils,

51

filaments, 53, 505 rod, 50, 51 Axolotl, 338 Axoneme, 53, 54, 56

Asplanchna, 637 Assulina, 490 seminulum, 489, 490

Astasia, 11, 46, 79, 302, 881
klebsi,
laevis,

Axopodia, 50-51, 505 Axostylar filaments, 70, 77, 369, 407 Axostyle, 70, 333, 369, 379

B
Babesia, 14, 622, 625
argentina, 624

302 166

bigemina, 32, 622-624

bovis,

longa, 54

Astasiidae, 293, 302-303 Aster acanthion rubens, 693 Asterias glacialis, 776 rubens, 32, 693 Asterigerina, 502 carinata, 501

canis,

624 624

Babesiidae, 600, 622-626 Bacillidium, 676

criodrili,

677

limnodrili, 677

Asterophora, 555
philica, 553 Astomata, 690, 691-698

Bacteria vs Protozoa, 5, 9-10 Bacterium parapelomyxac, 441

Badhamia, 430 utricularis, 430

Baetis, 767

Astral rays, 155, 156, 158, 160 Astrangia danae, 789 Astrocystella, 536 lobosa, 535, 536 Astrodisculus, 510 radians, 509, 510

Baikalodendron, 867 Baikalophrya, 867 Balanitozoon, 710

gyrans, 710 Balanonema, 764 biceps, 764

Astrophrya, 865
arenaria, 864, 865 Astrophyga magnifica, 750 Astropyle, 516 Astrorhizidae, 496 Astrosiga, 339 Astylozoon, 850 fallax, 850, 851 Astylozoonidae, 850-852 Ateles, 612 geoffroyi, 735 Atelopus, 655 Athene noctua, 351 Atopodinium, 831 fibulatum, 830, 831 Atyaephrya desmaresti, 546 Audouinia lamarcki, 543 tentaculata, 576

Balantidial dysentery, 799 Balantidiopsis, 798 Balantidiosis, 799

Balantidium, 63, 798 caviae, 799

coli, 8, 9, 14,

16, 30,

798-799, 889-

890
duodeni, 797, 800 praenucleatum, 797, 800
suis,

799

Balantiodoides, 798 Balantiophorus, 763

Balanus amphitrite, 546 eburneus, 546

Ball-of-yarn stage, 152

Balladyna, 838
elongata, 837, 838

SUBJECT INDEX
Bankia, 779
Barbel, 648, 659, 676

923

Barbulanympha,
laurabuda, 410

42, 157, 158,

410

ufalula, 158, 410, 411 Barbus barbus, 648, 659 fluviatilis, 659, 676 plebejus, 659 Barracouta, 649 Barrouxia, 588 ornata, 587, 588 Basal plate, 58 Bat, 349 Beccaricystis, 537 loriai, 537 Bed bugs, 349 Beloides, 557 firmus, 556, 557 Benedenia, 694 Benedictia biacalensis, 777 limneoides, 777 Bertramia, 637 asperospora, 637 capitellae, 638 euchlanis, 638 Beta granules, 82 Beta particles in Paramecium, 230 Beta rays on Protozoa, 134 Bibio marci, 557 Bicosoeca, 341
kepneri, 341
socialis, 341, 342 Bicosoecidae, 339, 341-343 Biggaria, 750 bermudense, 749, 750

Blepharoconus, 718 cervicalis, 718 Blepharocoridae, 737, 752-753 Blepharocorys, 752 bovis, 751, 753 equi, 753 uncinata, 751, 753 Blepharoplast, 54, 56, 77, 157, 160, 228, 230 loss of, 55, 228, 230-231 Blepharoprosthium, 88, 717 pireum, 717, 718 Blepharosphaera, 718 intestinalis, 718 Blepharozoum, 719 zonatum, 718, 719 Blood-films, 899-901 Blue bird, 617 Boaedon lineatus, 584 Boderia, 476 turneri, 475, 476 Bodo, 23, 362
caudata, 362, 363 edax, 362, 363 uncinatus, 24 Bodonidae, 339, 362-365

Boeck-Drbohlav's media, 887 Boil-disease of fish, 648 Bolivina, 502 punctata, 501 Bombina bombina, 688 pachypa, 688

Bombyx

mori, 670, 671

echinometris,

Binary

fission,

7'49. 750 169-171

Biological control, 10

Boophilus annulatus, 622 Bos indicus, 819, 820, 821 Bothriopsis, 557 histrio, 556, 557 Botryoidae, 522
Botula californiensis, 782 Boveria, 63, 779 teredinidi, 778, 779

Biomyxa, 422 cometa, 422-423

vagans, 421, 422 Biotypes, 213, 225 Bird malaria, 614-617 Birds, 15, 351, 586, 592, 626, 893 Biriushibio, 670

Box
614-617,

Black birds, 586 Black flies, 620, 622, 668 Black-head of turkey, 9, 336 Blastocystis hominis, 463, 893 Blastodiniidae, 314, 321-324 Blastodinium, 321 spinulosum, 321, 322
Blastula, 6 Blatta orientaUs, 407, 544, 545, 676,

boops, 377, 688 Brachiomonas, 278 westiana, 278, 279 Brachionus, 637 Branchioecetes, 727 gammari, 726, 727 Brachiura coccinea, 698 Brassica, 433 Bresslaua, 747 vorax, 746, 747

Brevoortiana tyrannus, 584, 655

Brumptina paulista, 459 Bryophyllum, 725

vorax, 724, 725 Bryophrya, 747-748 bavariensis, 746, 748 Bryozoa, 670, 867, 877 Bubos, 357 Buccinum, 574 undatum, 574 Budding, 171-172, 863, 867, 868

800
BlatteUa lapponica, 545 Blattidae, 8 Blepharisma, 24, 45-46, 803 lateritium, 801, 803 persicinum, 801, 803 steini, 801, 803 undulans, 27, 79, 803-804

924
717 parva, 717, 718 Butschliella, 693 chaetogaslri, 693 opheliae, 692, 693 Butschliidae, 700, 717-720 Buffelus bubalis, 821 Bufo, 655, 686, 860 cognatus, 688 compactilis, 687 lentiginosus 687 marinus, 688 terrestris, 656 valliceps, 166, 688 vulgaris, 390 Bulbocephalus, 552 elongatus, 552, 553 Buliminidae, 502 Bullanympha, 385 silvestrii, 384, 385 Bullinula, 486 indica, 485, 486 Bundleia, 718 postciliata, 718
Biitschlia,
,

PROTOZOOLOGY
Callipus lactarius, 555
Callitriche,

434
397

Calonympha, 397
grassii, 396,

Caloscolex, 817 cuspidatus, 817, 818 Calospira, 794 minkiewiczi, 793, 794

Calymma, 516
Calyx, 160 Calyptotricha, 770 pleuronemoides, 770-771

Cambarus, 854, 857

Cambolopsis sp., 548 Camels, 349, 350, 817, 818, 820,822 Camelus dromedarius, 230, 817, 818, 820 Camerinidae, 501 Campanella, 854 umbellaria, 853, 854 Campascus, 484 cornutus, 488, 484 Camptonema, 508 nutans, 507, 508 Canary, 388, 601, 602, 615, 616 Cannibalism, 101, 440 Cannosphaera, 523 Cannosphaeridae, 523 Canthocamptus, 857 minutus, 857 Capillitium, 429 Capitella capitata, 638 Capsa, 779 Capsellina, 482 timida, 481, 482 Carabus, 554 auratus, 554 violaceus, 554 Carchesium, 11, 39, 856 granulatum, 46, 856, 857 polypinum, 856, 857 Carcinoecetes, 547 bermudensis, 547 calappae, 547 hesperus, 546, 547 mithraxi, 547 Cardita calyculata, 560, 779 Carina moschata, 377 Carinae, 841 Carotin, 90, 418, 420 Carp, 353, 357 Carteria, 281 cordiformis, 282 ellipsoidalis, 282 obtusa, 26 Carteriidae, 276, 281-283 Caryonide, 192 Caryospora, 587 simplex, 587 Caryotropha, 575 mesnili, 575 Cassidulina, 503 laevigata, 503

Bursaria, 39, 797 truncatella, 797, 798 Bursariidae, 796, 797-800

Bursaridium, 798 difficile, 797, 798 Bursella, 710 spumosa, 710 Buteo borealis, 586 swainsoni, 586 Buxtonella, 735 sulcata, 734, 735

Cabbage, 433 Cacajao, 612 Caduceia, 383

bugnioni, 384, 3S4 Caementella, 523
stapedia,

523

Caementellidae, 523 Caenis, 534

Caenomorpha, 800-801
medusula, 24, 801 Calanus finmarchicus, 324 Calappa flammea, 547 Calcareous test, 493 Calcarina, 502 defrancei, 503 Calcarinidae, 502 Calcium chlorophosphate, 121 phosphate, 121 Callicebus, 612 Callimastigidae, 369, 375-376 Callimastix, 375 cyclopia, 375 equi, 875, 376 frontalis, 375 Calliphora, 354, 452 erythrocephala, 452

SUBJECT INDEX
Cassidulinidae, 502 Castanellidae, 524

925

Castanidium, 524 murrayi, 524

Castration, parasitic, 32, 670-671 Cat, 226, 349, 450, 579, 586 Catabolic products, 120, 121, 122 Cat-bird, 617 Catenoid colony, 174, 326 Catfish, 278, 660, 709

Cephalopoda, 573, 694 Cephalothamnium, 361 cyclopum, 361 Ceratiomyxa, 433 fruticulosa, 431 Ceratiomyxidae, 432 Ceratium, 11, 326 fusus, 825, 326-327
hirundinella, 24, 223, 224, 325, 326 longipes, 825, 326
tripos, 325, 326 var. atlantica, 326

Catostomus, 357 commersonii, 658

Cattle, 32, 349, 350, 375, 388, 457, 577, 622, 624, 625, 717, 735, 751, 752, 753, 817, 818, 819, 820, 821,

822
Cattle fever,
9,

622, 624

Caudal

58 Caulicola, 858 vulvata, 858 Caulleryella, 563

cirri,

Ceratodinium, 320 asymmetricum, 319, 321 Ceratomyxa, 649-650 hopkinsi, 650, 651 mesospora, 650, 651 shasta, 650 Ceratomyxidae, 649-651
Ceratophyllus fasciatus, 346, 351

Ceratopogon, 678
'

pipientis, 562, 563 Cavia, aperea, 752 porcella, 344, 752

solstitialis,

557, 562-563

Ceratospora, 539
mirabilis, 539, 540 Cercaria tenax, 13 Cercocebus, 612

Caviomonas, 344 mobilis, 848, 344 Cebus, 612

Cell, 5

Cercomonas,

23,

364

Cell-aggregates, Protozoa as, 6 Cell-anus, 64, 84, 102, 107 Cell-organ, 5, 60-91 Cellobiase, 106 Cellulase, 106 Cellulose, 29, 47, 105, 276, 427

crassicauda, 24, 368, 365 longicauda, 24, 868, 365

Cercopithecus, 612 Cerithium rupestre, 560

Certesia, 843 quadrinucleata, 842, 843 Cervus canadensis, 822

Cenolarus, 522
primordialis, 521 Central capsule, 70, 505, 506, 516

motor mass,

63, 64,

65

Cestracion, 655 zygaena, 651 Cestus veneris, 794 Cetonia, 376

spindle, 157, 158

Chaenea, 714
limicola, 714, 715 Chaetodipterus fabor, 651 Chaetogaster, 693

Centrechinus antillarum, 750, 800

Centriole, 55, 154, 155, 157, 158, 159 Centrodesmose, 156, 157 Centromere, 159, 160

Centrophorella, 725 fasciolatum, 724, 725

lanceolata,

725

Centropyxis, 484
aculeata, 225, 483, 484 Centrosome, 157, 158

Centrosphere, 163 Cepedea, 40, 687

cantabrigensis, 686, 687
fioridensis,

688

hawaiensis, 687
obovoidea, 687

Cepedella, 784
hepatica, 784

Cephalin, 528 Cephalina, 530, 541-560

Cephaloidophora, 543 nigrofusca, 543 olivia, 542, 543 Cephaloidophoridae, 541, 543

Chaetognatha, 466 Chaetospira, 836 mulleri, 835, 836 Chagas' disease, 348, 349 Chagasella, 592 hartmanni, 592 Chalkley's solution, 882 Challengeridae, 523 Challengeron, 523 wyvillei, 524 Chaos prothens, 11 Chara, 434 Charon, 753 equi, 751, 753 Chelydra serpentina, 458 Chemical composition of water, 2325 stimuli, 132-133 Chemicals on cysts, 451-452 Chicken, 336, 375, 388, 393, 580-582, 583, 584, 617


926
605 Chilo simplex, 670 Chilodinium, 320 cruciatum, 319, 320 Chilodochona, 848 quennerstedti, 848
Chill
fever,

PROTOZOOLOGY
and

Chlamydomonas

continued paupera, 233 pseudoparadoxa, 232

Chlamydomyxa, 422
montana, 421, 422

Chlamydophrys, 480
stercorea, 24, 480,

Chilodon, 731 steini, 732

Chilodonella, 11, 21, 44, 78, 79, 731 caudata, 732 cucullulus, 24, 71, 145, 146, 147,

481

Chloraster, 283 0yrans, 3, 283 Chlorasteridae, 276, 283 Chlorella, 29, 121, 135, 744

732
cypini, 732, 733
fluviatilis,

Chlorine on cysts, 451-452

Chlorogonium, 279-280
elongatum, 26 euchlorum, 26, 280 teragamum, 26 Chloromonadina, 256, 306-307 Chloromyxidae, 651, 654-655 Chloromyxum, 654-655 leydigi, 172, 652, 655 trijugum, 652, 655 Chlorophyll, 89, 254 Choanocystis, 513 lepidula, 513, 514 Choanocystella, 536 tentaculata, 535, 536 Choanocystoides, 536 costaricensis, 535-536 Choanomphalus, 777, 778 Choanophrya, 875 infundibulifera, 875-876, 877 Chondriosomes, 46, 80-83, 113, 891 Chondropus, 422 viridis, 422 Chonotricha, 28, 690, 847-849 Chorophilus triseriatus, 687 Chromatin, 40, 42, 146 Idio-, 44 Test of, 42 Tropho-, 44 Chromatid, 159, 160 Chromatoid body, 447 Chromatophore, 29, 45, 89-90, 107, 250, 256, 293, 297, 706 Chromic acid, 576 Chromidia, 44-45, 472 Chromidina, 694 elegans, 694, 695

732 hyalina, 733

longipharynx, 733 rotunda, 733 uncinata, 145, 229, 30, 732-733 Chilodontopsis, 729
vorax,

729-730

Chilomastigidae, 369, 374-375 Chilomastix, 14, 374

bettencourti,

374

caprae, 374 cuniculi, 374 (jallinarum, 375

intestinalis,

374 375

mesnili, 16, 29, 374,

Chilomitus, 377
caviae, 376, 377 Chilomonas, 79, 273, 881

oblonga, 274

Paramecium,

26, 109, 118, 273-274,

882 Chilophrya, 712 labiata, 711, 712 utahensis, 711, 712 Chilostomellidae, 503 Chimpanzee, 799, 826 Chiridota, 538 Jams, 538, 539 Chironomus, 769 plumosus, 34 Chitin, 47, 48 Chiton, caprearum, 560 Chlamydoblepharis, 281 Chlamydobotrys, 288
stellata, 288, 289 Chlamydococcus, 277

Chromomeres, 146

Chlamydodon, 63, 731 mnemosyne, 729, 731 Chlamydodontidae, 728, 731-733 Chlamydomonadidae, 276-281 Chlamydomonas, 45, 89, 181, 276277
angulosa, 277 debaryana, 223, 224, 225 epiphytica, 277, 278 eugametos, 232, 233 globosa, 277, 278 gracilis, 277, 73

Chromonema, 160
Chromosomes,
233 Chromulina,
155, 156, 157, 158, 159, 160, 166, 167-169, 206, 231,
79, 257,

258

pascheri, 258, 259 Chromulinidae, 257, 258-262 Chrysamoeba, 258 radians, 258, 261 Chrysapsis, 258 sagene, 258, 259 Chrysarachnion, 267

monadina, 277 73 paradoxa, 232

',

Chrysemys

insidians, 267, 268 elegans, 458


SUBJECT INDEX
Chrysemys
927
continued

continued

Clathrulina

marqinata, 583 pict'a bellii, 874, 875 Chrysidella, 29, 274 schaudinni, 273, 274

Chrysidiastrum, 267 catenation, 267 Chrysocapsa, 269 paludosa, 266, 269 Chrysocapsina, 257, 269 Chrysococcus, 258 ornatus, 258, 259 Chrysomyia macellaria, 452

elegans, 513, 514 Clathrulinidae, 506, 513 Clausia, 693 C lausocalanus arcuicornis, 321 furcatus, 321, 794 Cleaning glass-wares, 890 Cletodes longicaudatus, 867, 871

Cleveland-Sanders' medium, 888

Clevelandella, 809-810 panesthiae, 809, 810 Clevelandellidae, 790, 809-810 Clevelandia, 809 Cliff swallow, 617

Chrysomonadina, 256-269
Chrysopyxis, 260 cyathus, 259, 260 Chrysosphaerella, 260 lonqispina, 259, 260 Chrysothylakion, 267, 269 vorax, 268, 269 Chytriodinium, 323 parasiticum, 321, 323 Cilia, 55-57, 683 Ciliary field, 56 flagella, 53 movement, 127-129 zone, 56 Ciliata, 12, 249, 250, 683-862, 883 Cilioflagellata, 310
Ciliophora, 55, 349, 683-878 Ciliophryidae, 506, 508 Ciliophrys, 508 infusionum, 508, 509

Climacostomum, 807
virens, 24, 807, 808 Cliola viqilax, 660 Clitellis, arenarius, 662

Clupea harengus, 655 pilchardus, 658 Clymenella torquata, 323, 852 Clypeolina, 487 marginata, 485, 487 Cnidosporidia, 526, 643-682
Coccidia, 14, 15, 185, 527, 570-598 Coccidiosis, 9, 580

Coccidium, 577 oviforme, 577 Coccolith, 48

Coccolithidae, 257, 266-267

Coccomonas, 279
orbicularis, 279,

280

Coccomyxa, 658
morovi, 657, 658 Coccomyxidae, 655, 658

marina, 508 Ciliospore, 176 Cinetochilum, 765 margaritaceum, 24, 764, 765

Cocconema, 676
Coccospora, 676
slavinae, 676,

Cingulum, 326 Ciona intestinalis, 674, 785, 845 Circoporidae, 524 Circoporus, 524 octahedrus, 524 Circular cytostomal fibrils, 68, 69 Circum-oesophageal ring, 63 Cirri, 57-58, 683, 832
Cirrus fiber, 58, 65, 66
Citellus lateralis chrysodeirus,

677

Coccosporidae, 670, 676 Cochliatoxum, 826 periachtum, 825, 826 Cochliomyia, 354 Cochliophilus, 777
depressus, 777-778 Cochliopodium, 480

389

tridecemlineatus, 357, 457, 579 Citharichthys xanthostigmus, 651

Cladomonas, 358
fruticulosa, 358, 359 Cladonema radiatum, 790

bilimbosum, 480, 481 Cochlodinium, 320 atromaculatum, 319, 320 Cochlosoma, 377 rostratum, 376, 377 Cockroaches, 29, 363, 393, 407, 445,
449, 452, 453, 459, 462, 538, 544, 545, 638, 676, 800

Cladophora, 857 Cladothrix pelomyxae, 441 Cladotricha, 834 koltzowii, 833, 834
Clathrella, 511
foreli,

Codonella, 816
cratera, 815, 816 Codonocladium, 339 Codonoeca, 342 inclinata, 342

511,512

Clathrellidae, 506, 511

Clathrostoma, 742 viminale, 741, 742 Clathrostomidae, 737, 742 Clathrulina, 513

Codonosigopsis, 341 Codosiga, 339

disjuncta, utriculus,

339 339

Codosigidae, 339-341


928
Coelenterata, 693, 873, 877 Coelodendridae, 524

PROTOZOOLOGY
Colpoda
continued
cucullus, 24, 177, 178, 746

Coelodendrum, 524 ramosissimum, 524 Coelomonas, 306 Coelosoma, 713

Coelosomides, marina, 711, 713 Coelosporidium, 638 blattellae, 638 periplanetae, 637, 638
Coelotrichomastix convexa, 370 Coelozoic Protozoa, 30, 31, 109

duodenaria, 747

746 maupasi, 746-747 747 Colpodidae, 737, 745-748 Colponema, 364 loxodes, 363, 364 Columba livia, 619 Columbella rustica, 560 Colymbetes, 558 Cometodendron, 868
inflata,
steini, 34, 746,

Coenobium, 285
Cohnilembidae, 758, 771 Cohnilembus, 771 caeci, 770, 771 fusiformis, 770, 771 Colacium, 300-301 vesiculosum, 301 Coleorhynchus, 557 heros, 549, 556, 557 Colepidae, 700, 706-707 Colepismatophila, 548 watsonae, 546, 548 Coleps, 11, 46, 57, 706 bicuspis, 706, 707 elongatus, 706, 707 heter acanthus, 706, 707 hirtus, 706, 707 octospinus, 706, 707 spiralis, 706, 707
Collared Protozoa, 48, 339, 340, 341, 342, 343, 743, 759 Collecting canals, 84, 85, 86, 746 Collection of Protozoa, 879-880
Collinella,

clavatum, 866, 868

Cometoides, 554
capitatus, 553,

554

Commensal, 28-29 Commensalism, 28-29

nucleus, 42-44 Concentration of cysts, 894 Conchophthiridae, 774-776 Conchophthirus, 63, 84, 774 anodontae, 164-165, 774, 775 magna, 775 mytili, 76, 150, 776 Concrement vacuole, 87-55 Condylostoma, 806 patens, 806 vorticella, 805, 806 Condylostomidae, 796, 806 Cone-nosed bug, 349 Congo red, 103, 891 Conidophryidae, 738, 753-754 Conidophrys, 753-754 pilisuctor, 752, 753, 754 Conjugation, 13, 187-203, 690 Connochaetes taurinus, 457 Contractile canal, 85, 87

Compact

735

gundi, 734, 735

Collinia, 691

vacuole, 82, 83-85, 117,

118, 119, 125 Contractility, 60-62 Conus mediterraneus, 560 Copepoda, 321, 323, 324, 361, 674, 693, 867, 868, 870

Collodictyon, 371 triciliatum, 371, 373 Collosphaera, 522 Collosphaeridae, 522 Colonial Protozoa, 6, 255, 285-290

39,

173-174,

Copromastix, 374
prowazeki, 373, 374

Colony,
arboroid, 174, 342, 361 catenoid, 174, 326 dendritic, 174, 342, 361
discoid, 174, 2SS gregaloid, 174
linear, 174,

Copromonas, 303
303 Coprozoic Protozoa, 24, 436, 443 Coptolermes formosanus, 406, 414 Corbierea, 281 Corbula gibba, 786 Cordylophora lacustris, 865 Corky scab of potatoes, 434 Coronympha, 397 clevelandi, 396, 397 Corophium acherusicum, 753, 754 Corycacus venustus, 324 Corycella, 554 armata, 553, 554 Corycia, 479 coronata, 478, 480 Corythion, 489 pulchellum, 488, 489
subtilis, 182, 183,

326

spheroid, 174, 286, 289 Color of Protozoa, 45 water due to Protozoa, 311, 312, 320, 327, 706

Colpidium, 27, 762

campylum,

24, 26, 110, 761, 762 colpoda, 22, 56, 57, 761, 762 echini, 761, 762 striatum, 762

Colpoda,

11, 27, 44,

745-746

aspera, 24, 746, 747

SUBJECT INDEX
Costa, 71, 369
Costia, 33, 371
necatrix, 30, 372,

929

Cryptocercus punctulatus continued 393, 407, 409, 410, 411, 412, 413,

373

pyriformis, 372

Cota, 670 Cothurnia, 857 annulata, 857, 80S canthocampti, 857, 858 Cougourdella, 677

magna, 677-678
Coverglasses, 890, 901
bird, 615 Cranotheridium, 702 taeniatum, 701, 702 Crappie, 31, 660, 655

Cow

414 Cryptochilidium, 763 echini, 763, 764 Cryptochilum, 763 Cryptochrysis, 274 commutata, 273, 274 Cryptodifflugia, 479 oviformis, 478, 479 Cryptoglena, 300 pigra, 300

Cryptomonadina, 76, 256, 272-275 Cryptomonadidae, 272, 273-274 Cryptomonas, 273

ovata,

Craspedotella pileolus, 329

273
californica,

Craspedothorax, 739
Craspidochilus cinereus, 635 Craterocystis, 536 papua, 635, 536 Crayfish, 854, 857

Cryptomya

780

Crebricoma, 782 carinata, 782 kozloffi,, 781, 782

Crenilabrus melops, 633
ocellatus,

Cryptopharynx, 731 setigerus, 731, 732 Cryptops hortensis, 550 Cryptosporidium, 587 muris, 587 parvum, 588
Cryptotermes dudleyi, 379, 391
grassii,

397 393

638

hermsi, 381, 383, 393

longicollis,

paro, 638

Crepidula plana, 811 Crescent, 610 Cresta, 369, 380-381, 882

Cribraria, 432 aurantiaca, 431 Cribariidae, 431 Crickets, 363, 545'
Criodrilus, 696, 780

Cryptozoite, 602
Crystals, .720-121, 125, 442

Ctedoctema, 770
acanthocrypta, 770 Ctenocephalus canis, 353, 555 Ctenodactylus gundi, 625, 735

lacuum, 677
Cristigera, 769-770 media K 768, 770 phoenix, 768, 770 Crithidia, 345, 353 euryophthalmi, 353,
gerridis, 353,

Ctenophores, 794 Ctenosaura acanthura, 463 Ctenostomata, 23, 796, 829-831 Cubitermes, 445 Cucujus, 552 Cucurbitella, 484 mespiliformis, 483, 484

354

854

hyalommae, 353, 354

Crobylura, 714
pelagica, 714, 715 Crocodiles, 351 Cross-striation in cilia, 56, 57 Crossing over, 232-233

7, 600, 606, 615, 616, 668, 674 fatigans, 15 pipiens, 563, 602, 615, 617 Cultivation of

Culex,

Free-living Protozoa, 880-884 Parasitic Protozoa, 15-16, 450,

884-890
Cultures, Bacteria-free, 108, 109, 181, 343 Clone, 881

Crotaphytus collaris, 618 Cruciferous plants, 433 Crucinympha, 383 Crumenula, 299 Crustacea, 541, 546, 547, 558,
560, 691, 754, 866 Cruzella, 362

Mass, 881

Mixed, 881 Pure, 881, 884

559
Pure-line, 881 Stock, 881 Cunhaia, 822 curvata, 822, 823 Current vs Protozoa, 132 Cyathodiniidae, 737 Cyathodinium, 752 conicum, 752 piriforme, 751, 752 Cyathomonas, 274 truncata, 278, 274

Cryptobia, 357
borreli, 357, 358 cyprini, 357, 358 grohbeni, 357, 358 helicis, 357, 358 Cryptobiidae, 339, 357 Cryplocercus punctulatus,

29,

380,

930

PROTOZOOLOGY
Cytoplasmic division, 166, 169-174 binary fission, 169-171 budding, 171-172
multiple division, 171

Cyclidium, 24, 769 glaucoma, 57 litomesum, 768, 769 Cyclina sinensis, 111 Cyclochaeta, 860-861 domergui, 860, 861 spongillae, 860, 861 Cyclogramma, 728 trichocystis, 728, 729 Cyclonexis, 39, 265 annularis, 264, 265 Gyclonympha, 414 Cycloposthiidae, 814, 823-826 Cycloposthium, 70, 823-824 bipalmatum, 823, 824 dentiferum, 823, 824 Cyclops, 361, 375, 854, 870, 876 fuscus, 671 minutus, 859 ornatus, 876
Cyclosis, 11, 101

plasmotomy,

135,

172-173

schizogonv, 175, 526, 560, 599, 601

608, 609 Cytoplasmic inheritance, 238-243 mutation, 240 toxin, 238 Cytopyge, 64, 84, 102, 107 Cytostome, 59, 88, 101, 685 Cytozoic Protozoa, 30, 32, 109

Dacne

Cyclospora, 586
caryolytica, 586,

587

Cyclostoma elegans, 859 Cyclotrichium, 705-706

meunieri, 107, 683, 704, 705, 706

Cynomolgus, 456
Cynoscion regalis, 654 Cyphoderia, 24, 488 ampulla, 223, 488-489 Cyphon pallidulus, 548 Cypridium, 730 Cyprinus, 357 Cypris, 854 Cyrtocaryum, 794 halosydnae, 794, 795 Cyrtoidae, 522 Cyrtolophosis, 765 mucicola, 765, 766 Cyrtophora, 260 pedicellata, 259, 260
Cyst, 175, 176, 182, 226, 277, 447,
449, 638, 645, 748, 894
-carrier,

rufifrons, 547 Dactylochlamys, 23, 708 pisciformis, 707, 708 Dactylophoridae, 541, 550-552 Dactylophorus, 550 robustus, 550, 551 Dactylophrya, 873 roscovita, 872, 873 Dactylosaccus, 476 vermiformis, 475, 476 Dactylosoma, 625 ranarum, 624, 625 Dallasia, 761 Dallingeria, 370 drysdali, 370 Daphnia maxima, 674

Darkfield microscope, 52, 890, 891 Dasyhelea obscura, 540, 679 Dasypis novemcinctus, 349 Dasytricha, 751 ruminantium, 751 Deer mouse, Canadian, 351 Defecation process, 107, 108 Degeneration, 46

Deltopylum, 768-769 rhabdoides, 768, 769 Deltotrichonympha, 414 operculata, 414

Dendritic colony, 174, 342, 861

449

-passer, 449 viability of, 177, 450-453, 748

Cystidium, 522 princeps, 522 Cystobia, 539 irregularis, 540 Cystocephalus, 553 algerianus, 553 Cystodiniidae, 314 Cystodinium, 314 steini, 313, 314 Cystodiscus, 655 immersus, 655
Cystoflagellata, 312, 316, Cytochrome oxidase, 117 Cytogamy, 189, 204 Cytomere, 573, 575, 619

Dendrocoelum lacteum, 767 Dendrocometes, 867 paradoxus, 866, 867 Dendrocometidae, 863, 867-868 Dendrocometides, 867 priscus, 866, 867

Dendromonas, 361
virgaria, 361

Dendrorhynchus, 550
systeni, 550,

551

Dendrosoma, 864, 870

radians, 864, 865 Dendrosomidae, 863, 864

329

Cytopharynx, 685 Cytoplasm, 45-46

Dendrosomides, 866 paguri, 864, 866 Depression slide, 890 Derepyxis, 263 amphora, 263 ollula, 263

SUBJECT INDEX
Dermacenler reticulatus, 624 Dermestes lardarius, 557 Dero limosa, 590 Deroceras agreste, 388, 760 Deropristis inflata, 393 Derrengadera, 351 Desmarella, 340 irregularis, 340 moniliformis, 340 Desmose, 157, 160, 163 Desoxyribose nucleic acid, 151, 238 Deutomerite, 528 Devescovina, 77, 381
lemniscata, 381, 382

931

Digestive tubule, 101-102 Dileptus, 63, 725-727 americanus, 726, 727

anser, 44, 73, 148, 726, 727 Dimensions of Protozoa, 39 Dimorpha, 335 mutans, 335, 836 Dinamoeba, 440 mirabilis, 489, 440 Dinenympha, 78, 79, 379 fimbriata, 379, 380 gracilis, 379, 380 Dinenymphidae, 370, 379-380 Dinobryon, 265 divergens, 265 sertularia, 264, 265 Dinoflagellata, 114, 256, 310-32 9 Dinomonas, 360 vorax, 359, 360 Dinophysidae, 325, 328-329 Dinophysis, 328 acuta, 328, 329

42,

44,

Devescovinidae, 370, 380-385 Dexiotricha, 765 Dexiotrichides, 765 centralis, 765, 766 Diadema setosum, 800 Diaphoropodon, 487 mobile, 485, 487 Diaptomus castor, 674 Diastase, 106 Diastole, 83 Diatoms, 422 Dichilum, 763 cuneiforme, 763, 764
Dicnidia, 670, 678 Dicotylus, 768

Diophrys, 843
appendiculata, 148, 842, 843 Dipeptidase, 106 Diphasia attenuata, 873 Diphasic amoebae, 435, 883

Dictyophimus, 522 hertwigi, 522

Dictyostelium discoideum, 433 Dictyosteliidae, 433

Diplochlamys, 482 leidyi, 481, 482 Diploconidae, 520 Diploconus, 520

Diplocystidae, 531, 538 Diplocystis, 538 schneideri, 537, 538

Didelphys virginiana, 349 Didesmis, 717 quadrata, 718

Didiniidae, 700, 703-706

Didinium, 703
balbianii, 704, 705 nasutum, 27, 72, 111, 179, 206, 704-705 Didymiidae, 430 Didymium, 431 effusum, 480 Didymophyes, 544 gigantea, 544 Didymophidae, 541, 544 Dientamoeba, 444, 453, 454, 462 fragilis, 29, 337, 462-463 Difflugia, 45, 482, 883 arcula, 483 constricta, 483 corona, 225, 484 lobostoma, 483 oblonga, 482-483 pyriformis, 482
spiralis, 122 urceolata, 483 Difflugiella, 479

Diplodinium, 819-820 dentatum, 819, 820 ecaudatum, 822 Diplogromia, 472 Diplomita, 359 socialis, 359 Diplomonadina, 39, 369, 392-396 Diplophrys, 475 archeri, 475 Diploplastron, 820 affme, 819, 820 Diplopoda, 548 Diplosiga, 341 francei, 340, 341 socialis, 340, 341 Diplosigopsis, 341 afflnis, 341, 842 Diplostauron, 279 pentagonium, 278, 279 Direct nuclear division, 145-154 Discoid colony, 174, 288 Discoidae, 522 Discolith, 266

apiculata, 478, 479 Difflugiidae, 472, 482-487 Digestion, 82, 102-106

Discomorpha, 829-830 pectinata, 830 Discomorphidae, 829-830 Discophrya, 875 elongata, 875, 876 Discophryidae, 863, 875-877

932
Discorbis, 502 opercularis, 494 petalliformis, 495, 496 vilardeboanus, 496

PROTOZOOLOGY
Ducks, 377, 393, 588, 616, 620, 641 Dumatella carolinensis, 617 Dyes, 228, 896-899, 900-901 Dysdercus ruficollis, 592 Dysentery amoeba, 449 Dysmorphococcus, 284 variabilis, 282, 284 Dysteria, 730 calkinsi, 729, 730 lanceolata, 730 Dysteriidae, 728 Dytiscus marginalis, 855

Discorhynchus, 555
truncatus, 555, 556 Discosoma, 867 tenella, 866, 867 Discosphaera tubifer, 266, 267 Disematostoma, 759 butschlii, 759, 760 Dissodinium, 329 lunula, 828, 329 Dissosteria Carolina, 544 Distephanus speculum, 266, 267 Distigma, 304 proteus, 304, 305 Ditoxum, 826 funinucleum, 825, 826 Division, 145-166, 169-174 cytoplasmic, 166, 169-174 nuclear, 8, 145-166 Dixippus morosus, 34 Dobell-Laidlaw's media, 887-888 Dobellia, 576 binucleata, 576 Dobelliidae, 571, 576 Dobellina, 463 mesnili, 463, 465 Dog, 349, 350, 356, 395, 457, 579, 586, 624 Dogielella, 78, 79, 693 minuta, 692, 693 renalis, 693 sphaerii, 692, 693 Virginia, 692, 693 Dolichodinium, 327 lineatum, 327, 328 Donax, 576 trunculus, 637 vittatus, 852 Donkey, 349, 350, 351 Dorisiella, 586-587 scolelepidis, 587 Dorsal motor strand, 63 Dosinia bilnulata, 111 exoleta, 786

Earthworm,

531, 532, 533, 534, 691,

696, 697, 698, 779 Ebalia turnefacta, 848

Echinodermata, 693, 741, 748, 749, 750, 762, 763, 769, 771, 800 Echinomera, 550
magalhaesi, 550, 551 Echinometra lucunter, 750 oblonga, 800 Echinometris subangularis, 750, 800 Echinocystis, 534 globosa, 534 Echinospora, 588 labbei, 587, 588 Echinus esculentus, 750 lividus, 763 Ecology, 20-35 Ectocommensals, 28-29, 33 Ectoparasites, 29, 30, 33 Ectoplasm, 46 Eel-grass, 418 Eels, 353 Effect of parasites on hosts, 30-33, 347-348, 349, 355-356, 446, 605606, 607-608, 648-649, 799 Egg-yolk-saline medium, 888 Eimeria, 577 acervulina, 578, 582 adenoeides, 583 amydae, 583 anseris, 583 arloingi, 511 bovis, 577 brevoortiana, 578, 584 canis, 578, 579 caviae, 579 chrysemydis, 583 citelli, 578, 579 clupearum, 578, 584 cylindrica, 577 cynomysis, 578, 579 debliecki, 578, 579 dispersa, 583 ellipsoidalis, 577, 578 falciformis, 578, 579 faurei, 575, 577 felina, 579 gadi, 584 intricata, 577-579

Double forms, 235, 236

Dourine,

153,

191,

228,

229,

9, 351 Dove, 388, 615 Drehkrankheit, 649, 658 Drepanoceras, 739 Drepanomonas, 739 dentata, 738, 739 Drosophila, 678

confusa, 354

Drug-fast Protozoa, 228 Drug-resistant Protozoa, 228 Duboscqia, 674

legeri,

674-676
323

Duboscqella, 323
tintinnicola, 322,


SUBJECT INDEX
Eimeria
continued labbeana, 583 maxima, 578, 582
meleagridis, 583 meleagrimitis, 583 mephitidis, 578, 579 mitis, 578, 582 miyairii, 678, 579 monads, 578, 580
necatrix, 583 nieschulzi, 579
os,

933

Enchelyodon, 715-716 californicus, 716 Enchelyomorpha, 708

vermicularis, 707, 708

Enchelys, 714 auduboni, 714

Encystment,

curvilata, 714, 715 44, 175-177, 277,

744-

745, 748, 889

Endamoeba,

34,

444

blattae, 29, 49, 79, 150,

444-445

580

disperata, 445

oxyspora, 583 perforans, 575, 577

perforoides,

granosa, 445
lutea,

445

580

majestus, 445, 446'

pellucida, 445 sabulosa, 445

praecox, 583 prevoti, 578, 583 ranae, 575, 583 ranarum, 578, 583 sardinae, 578, 583-584 scabra, 579 schubergi, 570-571, 577 separata, 579 smithi, 577 stiedae, 13, 575, 577 teneHa, 575, 580-582 truncata, 583

simulans, 445, 446" suggrandis, 445 thomsoni, 445 vs Entamoeba, 444

Endamoebidae, 435, 443-465 Endocommensalism, 28, 29, 34

Endolimax, 444, 460-461 blattae, 462 caviae, 461 clevelandi, 461, 462 gregariniformis, 462
nana, 29, 453, 454, 461 ranarum, 462 Endomixis, 151
Endoparasites, 29, 30, 34, 35

wenyoni, 584
xoyomingensis, 577 zilrnii, 577 Eimeridea, 570-589 Eimeriidae, 571, 576-589 Eisenia foetida, 697 lonnbergi, 698, 779 Elaeorhanis, 510 cincta, 505, 510 Elaster, 513 oree$, 513, 514 Electrical stimuli vs Protozoa, 135136 Electron micrographs, 53-54, 56, 7.3-

Endoplasm, 46
Endoskeleton, 70

Endosome,

40, 41, 42, 44, 74,

163-164

Endosphaera, 873
engelmanni, 24, 852, 873, 876

Eleodes, 552

Elephant, 350
Eleutheria dichotoma, 693 Ellipsoidina, 502 Ellipsoidinidae, 502 Elliptio complanatus, 774, 775 Ellobiophrya, 852 donacis, 852, 555
Ellobiopsis, 324 chattoni, 322, 324 Elphidium, 11, 49, 501 crispa, 495 strigilata, 60, 501

Elytroplastron, 821
hegneri, 821

Embadomonas, 362 Emetin hydrochloride, 452

Emicronucleate
ciliates,

Enerthecoma, 784 kozloffi, 783, 784 Enoploplastron, 822 triloricatum, 821, 822 Entamoeba, 42, 444, 446 apis, 459 aulastomi, 459 barrel, 458, 886-887 bows, 457 buccalis, 455 caprae, 457 caviae, 457 CTteZft, 457, 4^5 cobayae, 457 coZz, 14, 29, 453-455, 555 cuniculi, 457 debliecki, 457, 455 eani, 457 gallinarum, 457 gingivalis, 14, 455-457 gedoelsti, 457
histolytica, 8, 14, 15, 16, 22, 27, 30,

153-154

Emys

592 Enchelydium, 702 fusidens, 701, 702

orbicularis,

49, 101, 176, 454, 887-889

intestinalis,

226,

446-453,

457

invadens, 41, 458-459, 887


934

PROTOZOOLOGY
Erastophrya, 865 chattoni, 864, 865 Eremoplastron, 820 bow's, 3i, 820 Eriphia spinifrons, 559 Ervilia, 730 Erythroblast in malaria, 615 Erythrocebus, 612 Erythrocytic schizogony, 599, 608, 609 Erythropsis, 316 cornuta, 315, 316 Eschaneustyla, 833-834 brachytona, 833, 834 Esox, 655 lucius, 353 reticulatus, 353 Espejoia, 763 mucicola, 763, 764 Espundia, 357 Eucamptocerca, 730 longa, 729, 730 Euchaeta japonica, 868 Euchlanis, 638 Euchrysomonadina, 257-267
Euciliata, 44, 685,

Entamoeba
ovis,

continued minchini, 459 muris, 457, J+58

457

paulista, 446, 459 phallusiae, 459 polecki, 457

ranarum, 459 terrapinae, 458 testudinis, 458 thomsoni, 459 venaticum, 457 Enterocystis, 533 ensz's, 532, 534 Enterohepatitis, 336 Enteromonas, 372-373 caviae, 373 hominis, 373, 375 Entodinium, 817-818 bursa, 818 caudatum, 818 Entodiscus, 749 borealis, 749 indomitus, 749 Entorhipidiidae, 737, 748-750 Entorhipidium, 63, 748 echini, 749 Entosiphon, 304-305 ovatum, 305 sulcatum, 305

601,

690-861

Eucomonympha, 414
imla, 413, 414

Eucomonymphidae,
maggii, 819, 820

Enzymes

in Protozoa, 82,

104, 105,

405, 414 Eucryptomonadina, 272-275 Eudiplodinium, 820

106 vs mating types, 197

Eudorina, 290
Euglena,
elegans, 134, 185, 289, 290, 11, 21, 24, 53, 294 acus, 294-295 deses, 26, 295, 296 ehrenbergi, 295, 296 gracilis, 26, 54, 79, 113, 295,
bacillaris, 25 klebsi, 295, 296
g.

Eodinium, 819 lobatum, 819 Eosin test, 450 Epalcidae, 829 Epalxis, 829
mirabilis, 829, 330 Epeorus torrentium, 676 Ephelota, 877 coronata, 870, 377 gemmipara, 870, 873, 877 plana, 877 Ephelotidae, 863 Ephemera vulgata, 678 Ephestia kuhniella, 563 Epiclintes, 838 pluvialis, 837, 838 Epicone, 310 Epidinium, 822 caudatum, 821, 822 ecaudatum, 63, ^4, 32i, 822 Epimerite, 76, 528 Epiplastron, 822 africanum, 821, 822 Epistylidae, 850, 853 Epistylis, 853, 870 cambari, 858, 854 fugitans, 854 niagarae, 853, 854 plicatilis, 853 Epitheca, 310

420

296

oxyuris, 295-296 pisciformis, 26, 294, 295 rubra, 295, 296 sanguinea, 113, 294, 95, sociabilis, 295, 296
spirogijra, 295 terricola, 295, 296
tripteris, 295, 296 wWefe'a, 26, 294, 5

296

Euglenamorpha, 302
hegneri, 300, 302 Euglenidae, 293, 294-302 Euglenoid movement, 294 Euglenoidina, 43, 256, 293-306 Euglypha, 47 acanthophora, 178, 487 alveolata, 23, 487

488 mucronata, 488 Euglyphidae, 472, 487-490 Eugregarinina, 527, 528-560 Eulophomonas, 408
cristata, 487,


SUBJECT INDEX
Eulophomonas
con fin ued
kalotermitis, 408 Eumycetozoa, 430-433 Eunicea crassa, 844 Eupagurus berhardus, 794 cuanensis, 866 excavatus, 866 Euphorbia, 354 Euphorbiaceae, 353, 354 Euplotaspis, 844 cionaecola, 844, 845 Euplotes, 24, 44, 63, 839

935

Fabrea, 807
salina, 807,

808

aediculatus, 840, 841 carinatus, 841, 842 charon, 841, 842 eurystomus, 59, 65, 66, 840, 841
patella, 25, 65, 66,

147,

148,

Factors for distribution, 20-28 encystment, 175-176. 177 178 excystment, 178, 179 Faecal examination, 892-894 Faeces, collection of, 880 Fannia canicularis, 452 Fats, 105, 114, 892 Fatty acid, 105, 107 Ferments, 104 Fertilization cone, 185, 186 granules, 185, 186 Feulgen's nucleal reaction, 43, 44, 45, 55, 145, 243, 896
Fibrillar structures, 60-70 Filopodia, 49, 419, 472 Finch, 586 Fingers and toes in cabbage, 433 Firebrat, 548 Fischerina, 499
helix,

118, 147, 193, 194, 195, 196, 228, 229, 234245, 286, 839, 840

plumipes, 841 woodruff., 147, &$0, 841 Euplotidae, 832, 839-843 Euplotidium, 841 agitatum, 841, 842 Eupoterion, 63, 150, 777
pernix, 775, 777 Eurychilum, 763 actiniae, 763, 764 Euryophthalmus convivus, 353 Eurypanopeus depressus, 560

498
371, 592, 650, 657, 709,

Euryphagous Protozoa, 27
Eurysporea, 649-651 Eusattus, 552 Eutaenia, 377 Eutreptia, 301 marina, 300, 301-302 viridis, 800, 301 Eutreptiella, 301 Eutrichomastix, 376 axostylis, 376, 377 batrachorum, 376, 377 serpentis, 376-377 Eutyphoeus foveatus, 536 peguanus, 536 rarus, 536 spinulosus, 536 Evolution of Protozoa, 5, 33, 34, 35 Excretion, 118-122 Excretory canal, 87 pores, 85, 87 Excystment, 178-179, 277, 448, 450, 748 Exflagellation, 606 Exoerythrocytic stages, 15, 599, 602604, 614 Exoskeleton, 10, 47-48, 70, 472, 493 Exuviaella, 312 apora, 312 compressa, 312-313 marina, 312, 313 Eye-spot, 89, 90-91

Fischerinidae, 499 Fish, 9, 30, 31, 321, 353, 357, 372, 377, 393, 464, 583, 584, 638, 643, 644, 645, 648, 649, 651, 652, 653, 654, 655, 656, 658, 659, 660, 672, 676, 688, 710, 865, 893 Fixatives, 895

Acetic-formaldehyde, 899 Bouin, 895-896 Carnoy, 896 Flemming, 896 Methyl alcohol, 900 Osmium tetroxide, 896 Schaudinn, 895, 898 Sublimate-acetic, 896, 898 formaldehyde, 898 Zenker, 63 Flagellata, 12, 254 Flagella, 52-55, 128, 254, 310 Flavobacterium, trifolium, 443 Fleas, 351, 353, 555 Fleckenkrankheit, 670 Flies, 354, 449, 452, 620, 678 Foaina, 383 nana, 382, 383 Foettingeria, 75, 789 actiniarum, 789, 791
Foettingeriidae, 789-795
Folliculina, 11,
boltoni,

807-808

808

moebiusi, 808 producta, 808 Folliculinidae, 796, 807-809 Fonsecaia, 544 polymorpha, 542, 544

Fontana's staining, 899 Food capture, 97-101

vacuoles, 88-89, 101-106, 125

PROTOZOOLOGY
Food
of Protozoa,

27-28

Foraminifera, 10, 11, 29, 39, 49, 185,

223, 249, 418,

493-504

Forma, 817 Formaldehyde, 576

Fossil Protozoa, 10, 249

Gastrostyla, 27, 838-839 muscorum, 887, 839 Gastrula, 6 Gelatinous substance, 47, 48
Geleiella,

850
863, 867, 868

Fowls, 462 Fox, 349

Free-living Protozoa, 20-28 Frenzelina, 486 conformis, 672 reniformis, 485, 486 Fresh preparations, 890-894
Fritillaria pellucida,

Gemmation, 171-172, Gemmules, 172

323

Frogs, 14, 29, 393, 462, 625, 651, 723, 800,

335, 583, 656, 852,

352, 374, 377, 390, 586, 588, 591, 592, 686, 687, 688, 694,

860

Frontal

cirri,

58

membrane, 59 Frontonia, 23, 758

branchiostomae 758, 759 leucas, 41, 74, 758, 759 Frontoniidae, 758-767 Fulica atra, 584
,

Geneiorhynchus, 558 aeschnae, 556, 558 Genes, 146, 231, 239, 240, 241, 242 Genetics, 223-243 Genotypes, 226, 229, 235, 238 Geographical distribution, 20, 28 Geophiles, 550 Gerda, 852 Gerris, 353 remigis, 353 Giardia, 393 canis, 395 caviae, 395 duodenalis, 395 enterica, 393
intestinalis, 13,

393-395

lamblia, 393

Fuligo, 430

430 Fundulus, 658 Fungus, 443, 639, 641

septica,

muris, 395 ondatrae, 395 simoni, 395 Gibbonsia elegans elegans, 651 Gibbula adamsoni, 560
divaricata, 560 rarilineala, 560 stain, 239, 608 Gigantism, 109, 110

Furcilla, 281 lobosa, 280, 281

Furcula, 70 Fusiformis lophomonadis, 408

melolonthae, 376 Fusulina, 498 Fusulinidae, 498

Giemsa

Gigantochloris, 279 permaxima, 278, 279 Gigantomonas, 385 herculea, 384, 385 Glaucoma, 761-762
ficaria,

Gadus, 657
584 morrhua, 584 virens, 584
aeglefinis,

26
762

pyriformis, 34, 151

scintillans, 26, 761,

vorax, 760

Galleria mellonella, 34 Gallinula chloropus, 584 Gallus domesticas, 617 Gametes, 180-181, 231, 494, 599, 601 Gametocytes, 599, 601, 605, 609 Gammarus, 847, 859 locusta, 672, 848 pulex, 547, 672, 847, 867

Glenodiniopsis, 314

puteanus, 867 Gamocystis, 545 tenax, 542, 545 Ganymedes, 541

anaspides, 540, 541

Ganymedidae, 531, 541

Gargarius, 787
gargarius, 786, 787 Gastrocirrhus, 843 stentoreus, 843, 844

Gastrophryne, 686
Gastrosteus aculeatus, 672 pungitus, 672

Glenodinium, 314 cinctum, SIS, 314 edax, 313, 314 neglectum, SIS, 314 pulvisculum, SIS, 314 uliginosum, 313, 314 Globigerina, 503 bulloides, 503 Globigerinidae, 503 Globorotalia, 503 Globorotaliidae, 503 Gloeomonas, 279 ovalis, 278, 279 Glossatella, 852 piscicola, 865 tintinnabulum, 852, 853 Glossina morsitans, 348 palpalis, 345, 347 tachinoides, 345, 347 Glossosiphonia complanata, 552


SUBJECT INDEX
Glugea, 672 anomala, 671, 672 herlwigi, 668, 672
h. var.

937

canadensis, 672

Glugea

mulleri, 672 cyst, 32, 672

Glycera, 539 Glycogenosis substance, 29, 45, 106,

112, 113, 116, 447, 644, 821, 892 Glyptotermes, 381, 383 parvulus, 383 Gnats, 463 Gnu, 457 Goat, 374, 375, 457, 577, 625, 817, 820 Gobius minutus, 672 Goldfish, 357 Golgi apparatus, 77, 78-80, 85, 891 Goniobasis plicifera silicula, 784 Goniocoma, 780 macomae, 781 Goniodoma, 327 acuminata, 327, 328 Gonium, 39, 287 formosum, 287 pectorale, 287, 288 sociale, 287, 288 Gonocyte, 321 Gonospora, 539 minchini, 537, 539, 540 Gonostomum, 834 strenuum, 833, 834 Gonyaulax, 327

continued calkinsi, 802, 803 Gryllotalpa gryllotalpa, 363 Gryllus abbreviatus, 545, 547 americanus, 545 pennsylvanicus, 547 Guinea pig, 344, 351, 364, 373, 374, 377, 395, 457, 461, 579, 591, 752,

Gruberia

822

Gunda

Gullet, 685 segmentata, 694

Gurleya, 674
nova, 694 richardi, 673, 674 tetraspora, 678, 674 Guttuliniidae, 433

Guyenotia, 663
sphaerulosa, 662, 663 Gymnodiniidae, 314, 318-321 Gymnodinioidae, 313-324 Gymnodinioides, 75, 791 calkinsi, 791 Gymnodinium, 318

aeruginosum, 318, 81
agile, 318, brevis, 311

319 319

palustre, 318,

rotundatum, 318, 319

Gymnonympha, 412
Gymnophrys, 422 Gymnospore, 558, 559 Gymnostomata, 690, 700-735 Gynotermone, 181
Gyrinus natator, 554 Gyrocoris, 800 Gyrodinium, 320 biconicum, 819, 320 hyalinum, 319, 320 Gyromonas, 395 ambulans, 892, 395

apiculata, 327, 828 polyedra, 327, 328

Gonyostomum, 306
semen, 306, 307 Goose, 583

Gorgonosoma, 867
Gorilla,

826

Graphoderes bilineatus, 855 zonatus, 855 Grasshopper, 544, 545 Gravity vs Protozoa, 131-132 Gregaloid colony, 174 Gregarina, 62, 79, 544 blattarum, 529, 530, 542, 544 cuneata, 528
locustae, 542, 544 oviceps, 542, 544-545

rigida,

polymorpha, 545 545

Habitats of Protozoa, free-living, 20-28 coprozoic, 24 katharobic, 23 mesosaprobic, 23 oligosaprobic, 23 polysaprobic, 23 sapropelic, 23 Haemaphysalis, leachi, 624 Haematin, 605

Gregarines, 13, 14, 79, 528 Gregarinida, 62, 527-569 Gregarinidae, 541, 544-547

Haematochrome,
706

21, 90, 91, 276, 297,

Haematococcus, 277
pluvialis, 115, 277, 278 Haematocyst, 277 Haematoxylin, 102, 896, 897 Haemoglobinuric fever, 622 Haemogregarina, 591, 692 stepanowi, 592, 593 Haemogregarinidae, 590, 592-594 Haemopis sanguisuga, 459

Gromia, 472-473 fluvialis, 473, 474 nigricans, 473, 4^4 ovoidea, 473, 4?4 Gromiidae, 472-476 Grouse, 336, 616

Growth

factors, 112

Gruberia, 803

93S

PROTOZOOLOGY
Heliospora, 547 longissima, 547, 549 Heliozoa, 12, 23, 39, 50, 505-515
Helix, 14, 590 aspersa, 357 Helodrilus caliginosus, 535, 691 foetidus, 531, 532, 534 longus, 533, 535

Haemoproteidae, 600, 618-622 Haemoproteus, 15, 618 columbae, 619-620 lophortyx, 620 metchnikovi, 620 Haemosporidia, 527, 599-634 Haemozoin, 121, 605, 608 Hahnert's solution, 882-883 Halibut, 648, 652 wormy, 648, 652, 653 Halkyardia, 502 radiata, 503 Halkyardiidae, 502 Hallezia, 873 brachypoda, 872, 873 Halosydna gelatinosa, 794 Halteria, 24, 814 grandinella, 814, 815 var. chlorelligera, 814, 815 cirrifera, 814, 815 Halteriidae, 814-815 Halteridium, 618 Humster, 614 Hanging drop preparation, 890-900 Hantkenina, 502
alabamensis, 501 Hantkeninidae, 502 Haplosporidia, 635-638 Haplosporidian cyst, 638 Haplosporidium, 635 chitonis, 635, 637 heterocirri, 636, 687 limnodrili, 636, 637 nemertis, 636, 637 scolopli, 636, 637 vejdovskii, 636, 637 Haplozoon, 323 clymenellae, 322, 323 Haptophrya, 694
inichigancnsis, 87, 694, 695 virginiensis, 694 Haptophryidae, 694-696 Harpacticus gracilis, 794 Harpalus pennsylvanicus erythropus, 545 Hartmannella, 442-443 hyalina, 443 Hartmannula, 730 entzi, 329, 730 Hastatella, 850

Helops

striatus,

553

Hemicaryon, 189
Hemicellulose, 70 Hemicycliostyla, 834 sphagni, 833, 834

Hemidactylium scutatutn, 694 Hemidinium, 318 nasutum, 318, 819 Hemiophrys, 723 Hemispeira, 776 asteriasi, 775, 776 Hemispeiridae, 774, 776-779 Hemispeiropsis, 776 Hemitubifex benedii, 662 Hemixis, 151, 206 Henlea leptodera, 538 Henneguya, 660 exilis, 648, 659, 660 mictospora, 660 salminicola, 640 Hentschelia, 552 thalassemae, 551, 552 Hepatozoon, 592 muris, 591, 592-594 Heredity, 223-243 Hericia hericia, 679 Herpetomonas, 354 drosophilae, 354 miiscae-domesticae, 354 muscarum, 354 Herpetophrya, 693 astomata, 693
Herpobdella atomaria, 591 Herring, 584 Heterakis gallinae, 337 Heteranthera dubia, 434 Heterocineto.psis, 784
goniobasidis, 783, 784 Heterocirrus viridis, 636

Heterocoma, 785
hyperparasitica, 785 Heterodinium, 327 scrippsi, 325, 327

aesculacantha, 851

Hawks, 388, 586

Hedriocystis, 513 reticulata, 513, 514

Heterohelicidae, 501

Heleopera, 486
petricola, 1^85,

486

Helicosporidia, 643, 678-679

Helicosporidium, 678-679 parasiticum, 679 Helicostoma, 772 buddenbrocki, 770, 772 Heliochona, 847
scheuteni,
sessilis,

Heteronema, 304 acus, 23, 304, 305 mutabile, 304, 305 Hetrophrys, 510 glabrescens, 510 myriopoda, 509, 510
Heterophryidae, 506, 510 Heteroploidy, 190 Heterotricha, 790-811 Heterotrophic nutrition, 97-107 Hexacontium, 221

848 848


SUBJECT INDEX
939

H exacontiu m

contin ued aster acanthion, 221

Homarus gammarus, 558 Homotrema, 504

Homotremidae, 504

Hexaconus, 520 serratus, 520 Hexactinomyxon, 663

psammoryctis, 662, 663 Hexalaspidae, 520

Honey bees, 10, 459, 670 Hoplonympha, 410

natator, 410, 411

Hoplonymphidae,

404, 410-412

Hexamastix, 377
batrachorum, 376, 377
caviae,

377

Hoplitophrya, 696 criodrili, 696, 697 secans, 696

robustus, 377 termopsis, 376, 377

Hormones,

29, 181, 185,

380

Horse, 349, 350, 351, 376, 457, 625,

641, 717, 718, 719, 720, 750, 753, 823, 824, 826, 874

Hexamita, 392-393 rryptocerci, 392, 393 inflata, 23, 392, 393 intestinalis, 392, 393 meleagridis, 393, 394 periplanetae 393 salmonis, 392, 393 Hexamitidae, 392-396 Hippocampus, 657 Hirmocystis, 545 harpali, 545, 546 termitis, 545, 546 Hirstella sp., 618
,

Horse serum egg medium, 888 Host-parasite relationships, 32-33

Human

Protozoa, see

Man

Hyaline cap, 46, 125 layer, 46 Hyalobryon, 25, 265-266 ramosum, 264, 266 Hyalodiscus, 423 rubicundus, 421, 423 Hyalogonium, 281
klebsi, 280, 281 Hyaloklossia, 576

Histiobalantium, 771 natans, 770, 771 semisetatum, 770, 771 Histiona, 342 zachariasi, 342 Histomonas, 335, 463 meleagridis, 335-338, 462 History of Protozoology, 10-16 Histozoic Protozoa, 30, 31, 109 Histrio, 832 Hodotermes mossamhicus, 385 Hogue's media, 885 Hold-fast organellae, 76 Holocoma, 781 primigenius, 781 Holomastigotes, 79, 405 elongatum, 405 Holomastigotidae, 404, 405-407 Holomastigotoides, 406 hartmanni, 405, 406
tusitala,

158,

159,

160,

161,

162,

406, 408 Holophrya, 27, 708

pelseneeri, 576 aegyptium, 353 Hyalosphenia, 479 papilio, 478, 479 Hyalospira, 794 caridinae, 794, 795 Hyalospora, 545 affinis, 545 Hyalosporina, 548 cambolopsisae, 548, 549 Hi/bopsis kentuckiensis, 660 Hybridization, 231-238 Hydaticus, 557 transversalis, 855 Hydatina, 637 Hydra, 30, 464, 859 japonica, 464 magnipapillata, 464 Hydr actinia cchinata, 771 Hydramoeba, 33, 34, 464 hydroxena, 29-30, 464-465

Hyalomma

Hydrogen-ion concentration,
27, 82, 103-104, 116, 118 Hydrophilus piccus, 558, 875

20, 25-

simplex, 708, 711 Holophryidae, 700, 708-717

Holophryoides, 719 ovalis, 719 Holophytic nutrition, 107-108 Holosticha, 838 hymenophora, 837, 838 vernalis, 837, 838 Holothuria, 539, 779 nigra, 540
Holotricha, 690-795 Holozoic nutrition, 88

H ydroporus

palustris, 592 Hydrostatic organellae, 62

Hydrous, 554 ceraboides, 554 Hydrurus, 269

foetidus, 89, 266,

269

Hyla, 686
pickeringi, 687
regilla,

Homalogastra, 767 setosa, 766, 767 Homalozoon, 702

vermiculare, 701, 702

versicolor,

687 686 263

690, 758-772

Hymenomonas, 263
roseola,

Hymenostomata,

940

PROTOZOOLOGY
Infusoria, 11

Hyperammina, 497
sabnodosa, J+97

Hyperamminidae, 497
Hyperdevescovina, 383 calotermiiis, 383 Hypermastigina, 29, 70, 118, 157, 333, 404-414 Hyperparasitism, 35, 637, 653, 672, 674, 694 Hyphantria cunea, 670 Hypocoma, 784 parasitica, 784-785 Hypocomagalma, 780
pholadidis, 780, 781

Insignicoma, 782 venusta, 781, 782

Intoshellina, 696 poljanskyi, 695, 696 Intoshellinidae, 696-698 Iodamoeba, 444, 459-460 buischlii, 29, 453, 454, 460, 893
suis,

460

williamsi, 460

Iodine cyst, 460 Iodinophilous vacuole, 113, 644

Irritability,

130-136

Irritant substance, 312

Hypocomatidium, 782
sphaerii, 783 Hypocomella, 784

Iron oxide in Protozoa, 47 Isocomides, 783

mytili, 783 Isogametes, 180

phoronopsidis, 783, 784

Hypocomidae, 774, 784-785 Hypocomides, 782

mediolariae, 782, 783

Isogamy, 182, 183, 185

Isopoda, 754
Isoptera, 8, 29, 543, 545, 674, 885-886 Isospora, 585
belli,

Hypocomidium, 784 Hypocomina, 783-784

tegularum, 783, 784

585

bigemina, 584, 586

felis,

Hypocone, 310 Hypostomata, 700, 728-735 Hypothallus, 428 Hypotheca, 310 Hypotricha, 796, 832-845 Hypotrichidium, 834 conicum, 834, 835
Hysterocineta, 779
eiseniae, 778,

buteonis, 586 586, 587

hominis, 584, 585-586

lacazii,

586

lieberkuhni, 586, rivolta, 584, 586

587

586 Isotricha, 751

suis,
intestinalis, 62, 751 prostoma, 62, 751

779

Hysterocinetidae, 774, 779-780

Isotrichidae, 737, 751

Isselina,

776

Ichthyophthirius, 33, 708-709

multifiliis, 30, 709-710 Ichthyosporidium, 638 giganteum, 635, 636, 638 hertwigi, 638 Ictalurus furcatus, 656 punctatus, 648, 660 Idiochromatin, 44 Idionympha, 412 perissa, 411, 412 Iduna, 730 Idyaea furcata, 790 Iguana iguana rhinolopha, 618 Iguanas, 463 Ileonema, 60, 716

Ithania, 592 wenrichi, 592 Ixodes ricinus, 624

J
Janickiella, 383

717 716-717 694 Immortality, 208 Immunity, 32-33

ciliata, 716,

disper,

Illex,

Janus green B., 80, 891 red, 80 Jarrina, 584 paludosa, 584 Jaundice in dog, 624 Joenia, 409 annectens, 408, 409 Joenina, 4l0 pulchella, 410 Joenopsis, 410 polytricha, 410 Juncus, 434

Incidence of Entamoeba histolytica, 449 Incubation period of malaria, 604-

Kahlia, 834
acrobates, 834, 836 simplex, 133, 154

605 Independent assortment, 231, 232 Indirect nuclear division, 154-166

Infraciliature, 56, 66

Kala

azar, 15, 355 Kalotermes, 381 brevicollis, 390


SUBJECT INDEX
Kalotermes
clevelandi,

941

continued

397

emersoni, 397 flavicollis, 408, 409, 410 hubbardi, 383

insularis,

Labyrinthomyxa, 419 sauvageaui, 419, 420

Labyrinthula, 418
cienkowskii, 418, 419 macrocystis, 418-419

384 minor, 412

simplicicornis, 406, 410, 412

Labyrinthulidae, 418-420 Lacerta, 362

muralis, 594 Lachmannella, 694-695 recurva, 695 Lacrymaria, 23, 713 coronata, 714, 715 lagenula, 713-714, 715 olor, 24, 713, 715 Lada, 779 Ladopsis, 779 Laelaps echidninus, 594 Lagena, 501
striata, 501 Lagenaria, cougourda, 677 Lagenidae, 501

Karotomorpha, 374 bufonis, 374, 375

Kappa

particles, 230, 239, 240, 241

Karyolysus, 594
lacertarum, 591, 594 Karyomastigont, 379, 397 Karyophore, 62, 751 Karyosome, 40 Katharobic Protozoa, 23 Kentrochona, 847 nebaliae, 847, 848 Kentrochonopsis, 847 Kentrophoros, 725 Kephyrion, 260 ovum, 259, 260 Keramosphaera, 500 Keramosphaeridae, 500 Kerona, 11, 837 polyporum, 28-29, 837, 838 Keronopsis, 838 rubra, 837, 838 Khawkinea, 297 halli, 297 ocellata, 297
Killer race of

Paramecium,

196, 236,

238-241
Kinetonucleus, 55

Kinetodesma, 56, 75 Kinetosome, 54, 55, 56, 58,

74, 75

61, 63, 66,

Kinety, 56

Kinoplasm, 61, 62 Kirbyella, 379 Kissing bug, 349 Klossia, 590 helicina, 14, 590
Klossiella, 591

cobayae, 591 muris, 591

Lagenoeca, 342 ovata, 342 Lagenophryidae, 857, 859 Lagenophrys, 859 labiata, 858, 859 patina, 858, 859 vaginicola, 858, 859 Lagynophrya, 708 mutans, 708, 711 Lamblia, 393 Laminaria lejolisii, 420 Lampoxanthium, 520 pandora, 521 Lamprodrilus, 697, 698 Lampropeltis getulus, 458 Lankesterella, 588 minima, 587, 588 Lankesteria, 538 ascidiae, 674 culicis, 529, 530, 538 Larcoidae, 522 Lasea rubra, 560 Laverania malariae, 610 Lecanophrya, 870 drosera, 869, 870
Lechriopyla, 63, 70, 741 mystax, 74 Lecudina, 542
pellucida, 542, 543 Lecudinidae, 541, 542-543 Lecythion, 552 thalassemae, 551, 552 Lecythium, 675 hyalinum, 675 Leeches, 352, 459, 552, 588, 592 Legendrea, 703 bellerophon, 701, 703 Legerella, 591

Knop's solution 883

Kofoidella, 693 eleutheriae, 692, 693 Kofoidia, 412 loriculata, 412, 413 Kofoidiidae, 404, 412

Kofoidina, 543
ovata,

543

Korschikoffia, 280 guttula, 280, 281 Kreyella, 739

Kudoa, 655
clupeidae, 654, 655 thyrsites, 649, 654, 655

hydropori, 591-592 Legeria, 557-558 agilis, 556, 558

942
Leidyana, 547

PROTOZOOLOGY
Life-cycle of Actipylea, 517-518

erratica, 529, 546, 547 Leidyanidae, 541, 547 Leidyonella, 412 Leidyopsis, 412 Leishmania, 8, 30, 32, 345, 355, 886, 901 brasiliensis, 357 donovani, 15, 30, 355-356 infantum, 355

Adelea ovata, 589 Aggregata eberthi, 573-5 7

Apostomea, 789-790 Avian Plasmodium, 604 Babesia bigemina, 622-624 Chromulina, 257 Chrysomonadina, 257 Coccidia, 570-571
Discorbis patelliformis, 496 Eimeria schubergi, 570-571 tenella, 580-582 Elphidium crispa, 495, 496 Entamoeba histolytica, 447-448 Eugregarinina, 529-530 Foraminifera, 494-496 Haemogregarina stepanowi, 592, 593 Haemoproleus columbae, 619 Helicosporidium parasiticum, 679 I chthyosporidium

tropica, 117,

356-357

Leishmaniasis, 32, 355-357

Lembadion, 760
bullinum, 759, 760

Lembus, 771 Lemming, 580

Lentospora, 658 Lepidosiren paradoxa, 658 Lepismatophila, 548 thermobiae, 546, 548 Lepocinclis, 299 ovum, 299, 300 Lepomis, 660 humilis, 651 Leptochlamys, 480 ampxdlacea, 480, 481 Leptodactylidae, 8 Leptodactylus, 655 Leptodiscus medusoides, 329 Leptomonas, 345, 353
ctenocephali, 353,

giganteum,

635,

636
Lankesteria culicis, 529, 530 Leucocytozoon simondi, 621 Microsporidia, 180, 669

N yctotherus

Mycetozoa, 427-429 Myxosporidia, 644-645

cordiformis, 198-199

Pandorina morum, 185 Peneroplis pertusus, 500

354
424

Plasmodium

vivax,

599-600, 601

Leptomyxa, 423
reticulata, 25, 176, 423,

Radiolaria, 517-519
Schizocystis gregarinoides, 561

Leptopharynx, 739 Leptospironympha, 407 eupora, 405, 407

Leptotheca, 651
ohlmacheri, 204, 650, 651

Schizogregarinina, 560

Sphaeromyxa

sabrazesi, 646, 647 Spirillina vivipara, 494-496 Spirophrya subparasitica, 495 Stempellia magna, 669

Lepus cuniculus, 351

domesticus, 351 Lernaeophrya, 865 capitata, 864, 865 Lesquereusia, 479 spiralis, 478, 479

Stephanosphaera pluvialis, 183 Telosporidia, 527 Tetramitus rostralus, 372 Thelohania legeri, 180

Trypanosoma
lewisi,

cruzi,

349

gambiense, 345-347

Leucine, 121 Leuciscus rutilus, 660

346

Leucocytozoon, 620 anatis, 620 andrewsi, 622 bonasae, 622 simondi, 620-622 smithi, 622 Leucophrys, 79, 760-761 patella, 761 Leucosin, 113 Libinia dubia, 543 Liceidae, 432 Licnophora, 810-811 conklini, 809, 811
macfarlandi, 809, 811 Lichnophoridae, 797, 810-811 Lieberkuhnia, 99, 473
wagneri, 24, 473-475

Lightstimuli on Protozoa, 22-23, 133135, 196 Ligniera, 434

Limax flavus, 388 marginatus, 588 Limnodrilus arenarius, 696

claparedeanus, 677 hoffmeisteri, 663 udekemianus, 636, 661, 663 Limnoria liguorum, 754 Limpets, 777, 859 Linear colony, 174, 326 Lineus bilineatus, 636 Linkage, 232 Liocephalus liopygue, 539 Lionotus, 24, 79, 723 fasciola, 21, 24, 723, 724

SUBJECT INDEX
Lipase, 106 Lipocystis, 563 polyspora, 563, 565 Lipoid substance, 56, 78, 80, 107 Lipolytic substance, 106
Lucilia, 354, 452 caesar, 452 Lugol's solution, 52, 460,

943

892 Lumbricus castaneus, 531, 533, 534

/u6c?<s,531,532,533,534,

Liponyssus saurarum, 594 Lipotropha, 563 macrospora, 563, 564

Lithobiusforficatus, 551, 570, 577, 590 mutabilis, 589 Lithocircus, 522 magnificus, 522 Lithocolla, 508
globosa,

697
531, 532, 533 534, 691, 697 variegatus, 562, 696, 698 Luminescence, 114, 317, 318, 327
terrestris,

509

Lycogala, 432 miniatum, 431 Lycogalidae, 432 Lygosoma moco, 618

Lithocollidae, 506, 508-510 Lithocystis, 539 brachycercus, 539, 540

lankesteri,

Lymnaea

539

Littorina obtusata, 776 rudis, 776 Litmus, 102, 103 Lituola, 498 nautiloidea, 498 Lituolidae, 498

stagnalis, 872 Lynchia brunea, 620 capensis,* 620 hirsuta, 620 Uvidicolor, 620 Lytechinus variegatus, 750

M
Macaca irus, 612, 614 Macacus cynomolgus, 612-613
nemestrinus, 386 rhesus, 22, 387, 388 Machadoella, 565 triatomae, 565 Machilis cylindrica, 545 Mackerel, 584 Macoma balthica, 776, 781

Liver-agar-serum medium, 888 Lizards, 362, 588, 594, 617, 618 Lobitermes longicollis, 391 Lobomonas, 279 rostrata, 278, 279 Lobopodia, 49 Lobster, 572 Locke-egg media, 450, 887 Locke's solution, 887 Locomotor organelles, 49-60, 379 Loftusia, 498 Loftusiidae, 498 Loligo, 694 Longitudinal fibrils, 68-69 flagellum, 310 Long-lasting modification, 228-229 Lophius piscatoris, 668 Lophocephalus, 553 insignis, 553

Macrogamete, 181, 599, 601, 605, 606 Macrogametocyte, 599, 601, 605, 606
Macrohodotermes massambicus, 405 Macromastix, 370-371 lapsa, 370, 371 Macronuclear regeneration, 152, 153 reorganization, 148-151 Macronucleus, 145, 146, 147-154, 684, 690

Macrospironympha,
xylopletha, 405, 407 Macrotrichomonas, 383 pulchra, 882, 383 Macrozoares americanus, 655 Mactra solidissima, 786 sulcataria, 111 veneriformis, 111 Mai de Caderas, 350 Malacophrys, 762 rotans, 761, 762-763 Malacostraca, 324 Malaria, 14, 30-31, 607-608 aestivo-autumnal, 610 benign tertian, 608 malignant tertian, 610

Lophomonadidae, 404, 407-410 Lophomonas, 407

blattarum, 29, 77, 160, 163, 175, 407, 409, 886 407-408, 409, 886
igniti igniti,

striata, 29,

Lophortyx, 620

Lophura

617

Lorica, 47 Loricata, 850, 857-859 Loripes lacteus, 779 Lottia gigantea, 859

Loxocephalus, 150, 763-764 plagius, 764 Loxodes, 88, 727 magnus, 726, 121 vorax, 726, 727 Loxodidae, 723, 727-728 Loxophillum, 723-724 meleagris, 724 setigerum, 724, 725

mild tertian, 611 ovale, 611

quartan, 610
subtertian, 610
tertian,

608

Malarial organisms of
Birds, 614-617


944
Malarial organisms of Man, 608-612, 613

PROTOZOOLOGY
continued

Monkeys, 612-614 Reptiles, 617-618

Malaria therapy, 608 Mallard duck, 620 Mallomonas, 258-259 litmosa, 259 Man, Protoza in, Balantidium coli, 8, 798-799
Chilomastix mesnili, 29, 374, 875 Dientamoeba fragilis, 29, 462-463 Endolimax nana, 29, 461 Entamoeba coli, 29, 453-455 gingivalis, 455-457 histolytica, 8, 446-453 Enteromonas hominis, 372-373 Giardia intestinalis, 393-395 Iodamoeba butschlii, 29, 460 Isospora hominis, 585-586 Leishmania brasiliensis, 357 donovani, 355-356 tropica, 356-357 Plasmodium falciparum, 610
malariae, 610-611
ovale,

Mastigophora, 12, 42, 249, 250, 254414 Mastigosphaera, 290 gobii, 289, 290 Mastotermes darwiniensis, 371, 414 Mating behavior, 192-193 type, 145, 192-196, 233 type determiner, 233-234, 236 type substance, 197, 235 Mattesia, 563 dispora, 563, 564 Maupasella, 696 nova, 696, 697 Maurer's dots, 605, 609, 610 Mayflies, 676, 678, 767 Meal worm, 545, 561 Mechanical stimuli on Protozoa, 130131 Media, culture, 881-890 Mediolaria marmorata, 782 Medusetta, 524
ansata, 524 Medusettidae, 523 Medusochloris, 283 phiale, 283 Megacyclops viridis, 676, 677-678 Megalosphaeric generation, 494, 495 proloculum, 494 Megamoebomyxa, 423
argillobia,

vivax,

611-612 608-610

Retortamonas intestinalis, 363-364 Sarcocystis lindemanni, 639-640 385-386, hominis, Trichomonas 387, 388 tenax, 386, 387
vaginalis,

423-424

Meiosis, 160, 206-208, 234, 496

gametic, 206-207, 234

zygotic, 208, 573, 574, 575

Trypanosoma

cruzi,

386-387 348-349

gambiense, 345-347
rhodesiense, 348

Melanin, 121 Melanoplus, 545

91, 316 Melolontha, 376, 557 melolontha, 377 Melophagus ovinus, 350

Melanosome,

Margarita, 432 Margaritidae, 432

Margarnia pyloalis, 670 Margaropus annulatus, 622 Marginal cirri, 58 Marmota monax, 580
Marsupiogaster, 306 picta, 805, 306 striata, 805, 306 Martinezia, 463 baezi, 461, 463 Maryna, 738 socialis, 738

Membrane,
cell,

46-47

nuclear, 40, 41, 42

Membranella, 59
basal plate, 59, 65
fiber,

65
65

fiber plate,

Marynidae, 737, 738-739 Massive nucleus, J+l, 42-44 Massartia, 320 nieuportensis, 819, 320 Mastigamoeba, 23, 334 aspera, 334 hylae, 335, 336 longifilum, 334 setosa, 884, 335 Mastigamoebidae, 333-338 Mastigella, 335 vitrea, 334, 335 Mastigina, 334 Mastigoneme, 54

Membranosorus, 434 Mendelian inheritance, 231, 232 Menhaden, 584 Menoidium, 303 Menospora, 549
polyacantha, 549, 551 Menosporidae, 541, 549 Merganser, red-breasted, 620 Mergus serrator, 620 Meriirix meritrix, 111 Merocystis, 574 kathae, 574-575 Merogregarina, 561 amaroucii, 561, 562 Meroselenidium, 564 keilini, 564 Merozoite, 580, 581, 599, 601


SUBJECT INDEX
Mesenchytraeus flavus, 636 Mesnilel'la, 698 clavata, 697, 698 rostrata, 697, 698
Mesocricetus, auratus, 388, 614

945

Mesodinium, 705 acarus, 704, 705

pulex, 24, 704, 705 rubrum, 706 Mesojoenia, 410 decipiens, 410 Mesosaprobic Protozoa, 23 Mesozoa, 643 Metabolism, 39 Metachromatic granules, 114 Metacineta, 869 mystacina, 24, 869 Metacoronympha, 397 senta, 396, 397 Metacryptozoite, 602 Metacysticlae, 700, 703 Metacystis, 703 truncata, 703, 704 Metadevescovina, 383 debilis, 77, 382, 383 Metadinium, 820 medium, 819, 820 Metamera, 552 reynoldsi, 552 schubergi, 551, 552

Microjoenia continued pyrijormis, 409, 410 Microlynchia fusilla, 620 Micron, 39 Micronucleus, 41, 44, 684, 690 Micropterus dolomieu, 865 salmoides, 660 Microregma, 714 audoboni, 714, 715 Microrhopalodina, 379 Microscopical examination, 890-901 Microspheric generation, 494, 495 proloculum, 494 Microspirotrichonympha, 406 ovalis, 405, 406 porteri, 405, 406 Microsporidia, 7-8, 10, 14, 32, 39, 40,
643,

668-678

Metaphyra, 691-692
sagittae, 692 Metaradiophrya, 697 asymmetrica, 698 lumbrici, 697

Metazoa compared with Protozoa, Methyl cellulose, 891

green, 42, 43, 892 Methylene blue, 891 Metopidae, 796, 800-801

Metopus,
es,

63,

800

Microsporidian cyst, 668, 672, 675 Microsporidiosis, 10, 668 Microstomus pacificus, 651 Microtaeniella clymenellae, 323 Microtermes hispaniolae, 445 panamaensis, 445 Microthorax, 739 simulans, 738, 739 Microtus guntheri, 614 pennsylvanicus, 388 Microvelia, 353 Miescher's tube, 638 Miliolidae, 499 Milk weeds, 353, 354 Milky barracouta, 649 Mites, 592, 594, 618 Mithrax forceps, 547 Mitosis, 154-166 Mitraspora, 651 elongata, 651 Mixotricha, 371 paradoxa, 371 Mixotrophic nutrition, 109
Mobilia, 850, 859-861 Modifications, long-lasting, 228

circumlabens, 800, 801 116, 199-200, 201, 800, 801 fuscus 800, 801 sigmoides, 800 straitus, 800, 801

Metridium marginatum, 789 Microcometes, 473 paludosa, 473, 4~4 Microcorycia, 481-482 flava, 481, 482
Microcyst, 429 Microdissection, 65
Microfolliculina, 808 limnoriae, 808

Modiolus modiolus, 111 Moina rectirostris, 674 Mole, 586 Molgula manhattensis, 865
Mollusca, 357, 558, 573, 575, 576, 635, 693, 774-787, 852 Molting hormone on Protozoa, 185,

M onadenia fidelis,

380 357 Monadidae, 339, 360-361 Monas, 24, 127, 128, 360
elongata, 360, 361 guttula, 360, 361 socialis, 53, 360, 361
sociabilis,
vestita,

Microgamete, 15, 181, 599, 601, 605, 606 Microgametocyte, 599, 601, 605, 606 Microglena, 260 ovum, 260, 262 Microgromia, 473 socialis, 473, 474 Microjoenia, 410

360

360, 361

Monera, 39, 423 Monkeys, 349, 456, 602, 603, 612, 735 Monocercomonas, 377 Monocercomonoides, 377 melolonthae, 376, 311

946
Monochiluni, 763
frontatum, 763, 764

PROTOZOOLOGY
Mya continued
inconspicua, 780
irus,
secta,

Monocnidea, 670-678 Monocystidae, 531-534

Monocystis, 79, 81, 207, 531 lumbrici, 531, 532 rostrata, 207, 532, 533

780 780
40, 418,

nasuta, 780

Mycetobia, pallipes, 676

Mycetozoa,

427-434

532 Monodinium, 703 Monodontophrya, 696 kijenskiji, 695, 696 Monductidae, 541, 548 Monoductus, 548 lunatus, 546, 548 Monomastix, 716 Monomonadina, 369-392 Monophasic amoebae, 437, 883 Monopylea, 519, 522-523 Monosiga, 340 ovata, 340 robusta, 340 Morphology, 39-91
ventrosa, 531,

Mycterothrix, 739 erlangeri, 738, 739

Mylestoma, 830-831
bipartitum, 830, 831 Mylestomidae, 829, 830-831 129, 333 Myophrisks, 62 Myriapoda, 550, 589, 590 Myriophryidae, 506, 514-515 Myriophrys, 514-515 paradoxa, 514, 515 Myriospora, 576 trophoniae, 576 Mytilus edulis, 776, 777,782, 783, 787 galloprovincialis, 560 minimus, 558, 560 Myxamoeba, 427 Myxidiidae, 655-657 Myxidium, 655 immersum, 655-656, 657 kudoi, 656 liberkuhni, 172, 655, 657 lindoyense, 655 serotinum, 654, 656 Myxobilatus, 660 Myxobolidae, 655, 658-660 Myxobolus, 658 conspicuus, 659 intestinalis, 31, 660 orbiculatus, 659 pfeifferi, 648, 658-659 squamosus, 659, 660 Myxochrysis, 261 paradoxa, 261 Myxococcus, pelomyxae, 441 Myxocystis, 676 Myxoflagellate, 429 Myxogasteres, 427 Myxomonas, 385 polymorpha, 385 Myxomycetes, 427 Myxophyllum, 776 steenstrupi, 775, 776 Myxoproteus, 651 cordiformis, 651, 652 Myxosoma, 658 catostomi, 154, 644, 658 cerebralis, 648, 658, 659 funduli, 658 Myxosomatidae, 655, 658 Myxosporidia, 9, 14, 31, 40, 76, 643660 Myxosporidian cyst, 645, 648, 649, 653, 659 Myxotheca, 476 arenilega, 4^5, 476

Myonemes, 61-62,

Morphonemes, 63
Mosquitoes, 530, 538, 600, 606, 614, 615 Motella, 656, 657 mustela, 393 tricirrata, 393 Motorium, 63, 64, 65, 66, 68, 69

Mouse, 228, 349, 351, 374, 395, 457,

579, 587, 591, 614, 639, 641, 672

Movement by
cilia,

127-129
126-127, 128

flagella,

myonemes, 129-130

pseudopodia, 122-126 oxostoma breviceps, 659 Mrazekia, 676

caudala, 676, 677 Mrazekiella, 698 intermedia, 697, 698

Mrazekiidae, 670, 676-678 Mule, 349 Muller's law, 517

vesicle, 87, 88, 727, 728 Multicilia, 333 lacustris, 333, 334 marina, 333, 334 Multiciliidae, 333

Multifasciculatum, 875
elegans, 874, 875 Multiple conjugation, 202 Multiple division, 171 fission cyst, 494 Munia oryzivora, 351 Murrina, 351 Mus musculus, 349, 389, 591 Musca, 354, 678 domestica, 452 Musgrave-Clegg's medium, 883 Muskrat, 395 Mutation, 229-230, 240, 242 My a arenaria, 780

SUBJECT INDEX
Nadinella, 486 tenella, 485, 486
Nicollella, 734-735 ctenodactyli 734,
,

947

735

Nigrosin, 892

Nagana,

9, 14,

349

Nina, 550
gracilis, 528, 529, 550,

Naegleria, 436
gruberi, 24, 436 bistadialis, 436 Naegleriidae, 60, 435-436

551

Nitocra typica, 870

Nitrogen deficiency, 90 N N N Medium, 886

Noctiluca, 11, 39, 316-317 miliar is, 317 scintillans, 114, 315, 317-318 Noctilucidae, 314, 316-318

Naiadaceae, 418 Nassoidae, 522 Nassula, 79, 728

aurea, 24, 728, 729 Nassulidae, 728

Nasutitermes kirbyi, 377 Natrix cyclopion, 459 rhombifer, 459 sipedon, 459 s. sipedon, 459 Navicula, 277 Nebalia bipes, 324 geoffroyi, 792, 847 Nebela, 490 collaris, 489, 490 Necturus, 859

Nonionidae, 501 Nosema, 670 aedis, 671, 672 anophelis, 671 apis, 10, 32, 670-671
bombycis, 10, 14, 32, 670, 671 bryozoides, 670, 671
cyclopis, 671 lophii, 668 notabilis, 35,

Nematocyst, 76, 324 Nematocystis, 533

vermicularis, 582, 533

Nematode, 390, 674 Nematodinium, 316

partitum, 815, 316

Nematopsis, 558 legeri, 558-560 ostrearum, 560 panopei, 560 Nemertinea, 538

Neoactinomyxum, 663
globosum, 662, 663 Neosporidia, 526

653 Nosema-disease, 670, 671 Nosematidae, 670-676 Notila, 380 proteus, 380 Notosolenus, 305-306 apocamptus, 305, 306 sinuatus, 305, 306 Notropis blennius, 660 cornutus, 660 gilberti, 659 Nucleal reaction, Feulgen's, 897-898 creft, Nuclear 147 Nuclear division, 145-166 direct, 145-154 indirect, 154-166 Nuclear membrane, 40
reorganization, 147-151, 152 sap, 40 Nuclearia, 421 delicatula, 419, 422 simplex, 422

Neotermes, 381, 383 connexus, 383 dalbergiae, 379 erythraeus, 385 greeni, 383 simplicornis, 378 tectonae, 379
Neotoina fuscipes annectens, 351 /. macrotis, 349, 351 micropus micro pus, 351

Nucleic acid, 42, 44, 115 Nucleolus, 40 Nucleophaga, 893 Nucleoplasm, 40, 41 Nucleus, 40-44, 684

Nepa

cinerea, 557, 563, 588 Nephroselmidae, 272, 274-275 Nephroselmis, 274 olvacea, 273, 274 Nereis beaucourdrayi, 543 cullrifera, 543 Net-plasmodium, 418

compact, 41, 42-44 r macro-, 41, 42, 43, 44, 684 Iflmicro-, 41, 44, 684 vesicular, 40-42 Nutrition, 97-116
v

Neuromotor apparatus, 63-66, 67-68,

69, 731

Neurophane, 61 Neusina, 499 Neusinidae, 499

Neutral red, 78, 79, 103, 104, 450, 528, 891 Newt, 352

autotrophic, 107 heterotrophic, 97 holophytic, 107-108 holozoic, 88, 97-107 mixostrophic, 109 parasitic, 109 phytotrophic, 107 sapropelic, 23 saprophytic, 108 saprozoic, 89, 108-109


948

PROTOZOOLOGY
Opercularia
continued
stenostoma, 853, 854 Operculariella, 854 parasitica, 853, 854-855

Nutrition continued zootrophic, 97 Nyctobates pennsylvanica, 555 Nvctotherus, 13, 804

cordiformis, 198, 199, 805-806 ovalis, 29, 42, 43, 44, 62, 147, 804,

805

Operculina, 501 ammonoides, 501 Ophelia limacina, 693 Ophiothrix fragilis, 793

Obelia commissuralis, 873 geniculata, 873 Ocean pout, 655 Ocellus, 91, 310, 316 Ochromonadidae, 257, 264-266

Ochromonas, 264
granulans, 264 ludibunda, 264
mutabilis, 264

Octolasium complanatum, 533 Octomitus, 392

Octomyxa, 434
Octopus letracirrhus, 694 Octosporea, 678 muscae-domesticae, 677, 678 Ocular micrometer, 891 Odor produced by Protozoa, 9, 114

Oikomonadidae, 339, 343-344 Oikomonas, 343 termo, 25, 28, 343

Oikopleura dioica, 321
Oil, 105,

113-114

Oligosaprobic Protozoa, 23
Oligotricha, 790, 814-826

Oncopeltus fascialus, 354

Ondatra zibethica, 395 Onychodactylus, 730 Onychodromopsis, 839 flexilis, 839, 840 Onychodromus, 839 grandis, 839, 840 Oocyst, 185, 571, 576, 599, 601 Oodinium, 321 limneticum, 321, 323 ocellatum, 321, 323 poucheti, 321, 322 Ookinete, 187, 599, 601, 621, 623
Oospira, 791 Opalina, 13, 40, 685-686
carolinensis, 687 chorophili, 687

hylaxena, 686
kennicotti,

687

obtrigonoidea, 686 oregonensis, 687 pickeringii, 687

spiralis,

687

Opalinidae, 685-688 Opalinopsidae, 694 Opalinopsis, 694

Opercular

sepiolae, 694, 695 fibers, 63 Opercularia, 854 plicatilis, 853. 854

Ophisthotrichum, 822 janus, 822, 823 thomasi, 822 Ophiurespira, 793 weilli, 792, 793 Ophrydiidae, 850, 852 Ophrydium, 39, 852 ectatum, 851, 852 sessile, 851, 852 vernalis, 851, 852 Ophryocephalus, 870 capitatum, 869, 870 Ophryocystidae, 560-562 Ophryocystis, 560-561 mesnili, 561, 562 Ophryodendridae, 863, 867 Ophryodendron, 867 belgicum, 866, 867 porcellanum, 866, 867 Ophryoglena, 767 atra, 768 collini, 766, 767 intestinalis, 766, 768 parasitica, 767 pyriformis, 766, 768 Ophryoglenidae, 758, 767-769 Ophryoscolecidae, 70, 119, 814, 816822 Ophryoscolecin, 70 Ophryoscolex, 817 bicoronatus, 817, 818 caudatus, 817, 818 quadricoronatus, 817, 818 Ophthalmidiidae, 499 Opisthodon, 723 Opisthonecta, 851-852 henneguyi, 851, 852, 873 Opisthostyla, 854 annulata, 853, 854 Opisthotricha, 832 Opossum, 349 Opsanus beta, 35, 653, 672 tau, 35, 653, 672 Oral basket, 71 groove, 685 membrane, 59 Orang-outang, 799 Orbitoides, 504 Orbitoididae, 504 Orbitolinidae, 499 Orbulina universa, 223 Orcadella, 432 operculata, 431 Orcheobius, 590 herpobdellae, 591

SUBJECT INDEX
Orchesiiu agilis, 691, 733
palustris,

949

733

Orchitophrya, 693
stellarum, 32, 692, 693 Orchopeas w. wickhami, 351

Palatinella, 260 cyrtophora, 259, 260 Paldina vivipara, 875 Palmathydra robusta, 4(54 Palmella stage, 257, 276, 277

Organellae, 5, 60-91 Oriental sore, 356 Origin of parasitism, 33-35 Orosphaera, 521 Orosphaeridae, 521

Pamphagus, 480
armatus, 23 mutabilis, 478, 480 Pandorina, 289-290 morum, 185, 289, 290 Panesthia javanica, 810 spandica, 810 Panopeus herbesti, 560 occidentalis, 560 Panorpa communis, 563 Pansporoblast, 187, 645 Panslrongylus megistus, 349 Pap snoek, 649 Papio, 612 Parabasal apparatus, 77-78, 333 body, 333, 369 Parabiotic twins, 191 Parablepharisma, 804 pellitum, 802, 804 Paracalanus, 693 parvus, 324, 794 Parachaenia, 780 myae, 780 Paracineta, 868
limbata, 868, 869

Orthodon, 730 hamulus, 729, 730

Orthognathotervies wheeleri, 388

Orthomorpha, 544 gracilis, 544

Oryctes, 376, 544
nasicornis, 544 Osmerus, 688 eparlanus, 672 mordax, 672 Osmiophile structures, 78, 79 Osmium tetroxide, 80 Ostracodinium, 821-822 dentatum, 821, 822 Ostrea virginica, 442, 560 Otus asio naevius, 617 Ovis orientulis cycloceros, 817 Ovivora, 572 thalassemae, 572, 573 Oxazin, 228

Oxidation, 116 Oxidase, 104, 117

Oxygen consumption, 116-118

on Protozoa,
29, 116-11!

Paraclevelandia, 810 brevis, 809, 810 simplex, 152 Paradesmose, 157

Oxmonadidae, 369, 378-379 Oxymonas, 378

dimorpha, 378
grandis, 378-379 Oxnerella, 508 muritima, 154, 155, 508

Paradevescovina, 383
Paradileptus, 727
conicus, 726, 727
estensis, 727 robustus, 726, 727 Paradinium, 324 poucheti, 822, 324 Paraellobiopsis, 324 coutieri, 822, 324 Paraeuplotes, 843 tortugensis, 843-844 Paraeuplotidae, 832, 843-845 Parafolliculina, 809 violacea, 808, 809 Paraglaucoma, 762 rostratu, 761, 762 Paraglycogen, 70, 112, 113, 116, 528 Paraholosticha, 838 herbicolu, 837, 838 Parahypocoma, 785 collini, 785 Paraisotricha, 750

Oxyphysis, 329
oxytoxoides, 328, 329 Oxyrrhis, 314 marina, 314, 315 Oxytricha, 23, 63, 832
bifaria, 832, 833 J fallax, 21, 832 , 833

hymenostomu, 153 ludibundu, 832, 833 883 Oxytrichidae, 832-839 Oyster, 442, 560 Owl, 617
setigera, 832,

Pace and Belda's solution, 883 Pachygrapsus, crassipes, 547

marmoratus, 672 transversus, 547 Paedogamy, 645 Paphia philippinarum, 111 Palacalanus parvus, 321 Palaemonetes, 791

beckeri, 750, 751 colpoidea, 750, 751 Paraisotrichidae, 737, 750 Paraisotrichopsis, 720 composita, 719, 720 Parajoenia, 381
grassii,

381-383


950
Parajulus venustus, 544 Paramaecium, 742 Parameciidae, 737, 742-745 Paramecin, 238

PROTOZOOLOGY
Pavonina
continued
flabelliformis, 501 Pebrine disease, 10, 14, 669, 670 Pecten, 31 maximus, 575 Pectinella, 56 Pedigree culture, 881 Pelamphora, 703 butschlii, 703 Pelatractus, 703 grandis, 703, 704 Pelecyophrya, 786 tapetis, 786-787 Pellicle, 46-47, 118, 435 Pelodinium, 829

Paramecium,

11, 22, 24, 56, 57, 63, 74, 79, 132, 179, 742, 745 aurelia, 26, 41, 44, 151, 152, 153, 190-191, 193-194, 196, 233,

236, 238, 241, 242, 743 bursaria, 25, 26, 27, 29, 121, 154, 189-190, 192, 194-196, 202, 743, 744 calkinsi, 24, 27, 196, 748, 744

caudatum, 20, 21, 22, 25, 26, 44,

117,
118,

72,

119, 120,

145, 146,

187-189, 225, 227, 228, 237, 742-743, 745 multimicronucleatum, 21, 25, 27, 28, 67, 68, 69, 85, 86, 191, 743, 744 poltcaryum, 27, 743, 744 putrinum, 743, 744 trichium, 27, 190, 743, 744
woodruffi, 27, 743, 744

reniforme, 829, 830

Pelomyxa,

40, 42, 440 carolinensis, 46, 49, 117, 135, 164, 173, 176, 441, 442, 883 illinoisensis, 46, 176, 44 1, 442 palustris, 23, 441

villosa, 441 Penardia, 423

Paramoeba, 465 pigmentifera, 465-466

schaudinni, 466 Paramoebidae, 435, 465-466

Paramylon, 105, 113, 203 Paranassula, 728 microstoma, 728, 729 Parapodophyra, 868 typha, 868, 869 Parapolytoma, 281
satura, 280, 281 Parasitic castration, 32, 670-671 Parasitic nutrition, 109 Parasitic Protozoa, 28-35, 116, 880 Parasitism, 29-32 origin of, 33-35

mutabilis, 421, 423 Penardiella, 702 crassa, 701, 702 Peneroplis, 499 pertusus, 48, 500

Peneroplidae, 499 Penniculus, 68, 69

Pentatrichomonas, 391 bengalensis, 391 Pentatrichomonoides, 391 scroa, 391 Pepsin-like enzyme, 106
Peptidase, 104, 106 Peranema, 46, 79, 304, 881
granulifera,

304

trichophorum, 54, 55, 81, 100,304,

Paraspathidium, 700
trichostomum, 700, 701 Paravorticella, 852 clymenellae, 851, 852 Paresis, 600

305
Perca fluviatilis, 353
Perezella, 692-693 pelagica, 692, 693 Perezia, 672-673 lankesteriae, 673, 674 mesnili, 673-674 Periacineta, 871 buckei, 872

Pareuglypha, 487 Parmulina, 482 cyathus, 481, 482 Parophrys vetulus, 651 Paroral cone, 191, 204 Paroxysm, 599, 605
Parthenogenesis, 285, 605 Passer domesticus, 586, 615 Passerine birds, 586, 615
Patellina, 502 corrugata, 496

Pericaryon, 794
cesticola, 792, 794 Peridiniidae, 325 Peridiniinea, 312, 313-329 Peridinin, 90 Peridinioidae, 313, 324-329

Peridinium, 326
divergens, 825, 326 tabulatum, 825, 326 Perioral membrane, 59

Pathological changes in host, 30-33, 347-348, 349, 355-356, 446, 605606, 607-608, 799
Paulinella, 488

chromatophora, 488
Pavillardia, 318
tentaculifera,

Peripheral granules of nucleus, 42 Periplaneta americana, 452, 453, 538 Peripylea, 519, 520-522
Perispira, 702 ovum, 701, 702 strephosoma, 701, 702

318

Pavonina, 502


SUBJECT INDEX
Peristome, 59, 685
Peristyle, 344 Peritricha, 28, 33, 61, 690, Peritromidae, 797, 810

951

Philaster continued armata, 770, 111

850-862

Peritromus, 810
californicus, 809,

digitiformis, 770, 771 Philasteridae, 758, 771-772 Philasterides, 771

810

Phlebotomus, 355
argentipes, 355, 356 intermedins, 357

emmae, 810 Permanent preparations, 894-901

Peromyscus, 389 leucopus, 388
maniculatus, 351

panamensis, 357
papatasii, 355, 357

Petalomonas, 302-303
mediocanellata, 802, 303 Petalostoma minutum, 576, 661 Petrocheliden I. lunifrons, 617
Pfeifferinella, 588 ellipsoides, 587,

588

impudica, 588 Phacodinium, 804

metschnicoffi, 801, 804 Phacotidae, 276, 284 Phacotus, 284 lenticular is, 282, 284 Phacus, 24, 297 acuminata, 298, 299 longicauda, 298 monilata, 298, 299 oscillans, 298, 299

357 Pholadidea penita, 780 Pholas crispata, 782 Phorcus, richardi, 560 Phoretrophrya, 791 nebaliae, 791, 792 Phormia, 354 Phormobothrys, 523 Phoronopsis viridis, 784 Phoront, 789, 790 Phosphorescence, 114, 317, 318, 327 Phosphorus deficiency, 90 Photogenic granules, 114 Photorophrya, 793 insidiosa, 792, 794 Photosynthesis, 23, 25, 90, 107, 108 Phryganella, 485
sergenti,

acropodia, 485-486

297-298 pyrum, 298 torta, 298, 299 Phaeocapsina, 272, 275 Phaeodium, 516 Phaeosphaera, 269 gelatinosa, 266, 269 Phaeolhamnion confervicoluni, 275 Phagocytosis, 602 Phalangium, cornutum, 556 crassum, 556 opilio, 556 Phalansteriidae, 339 Phalansterium, 339 digitatum, 339, 340 Phallusia mamillata, 459 Pharyngeal basket, 71 Phascolodon, 731
pleuronectes,
vorticella, 729,

Phrynosoma

asio,

618

cornutum, 618 Phycochrisin, 89

273,

731

Phase microscope,

52, 83, 891 Pheasant, 338, 583, 617 fire-back, 617 Phenol red, 103 Pheretima barbadensis, 533, 536 beaufortii, 536 hawayana, 536

Phycocyanin, 90 Phyllognathus, 544 Phyllomitus, 364 undulans, 363, 364 Phyllomonas, 280 phacoides, 280 Phylogeny of Protozoa, 249-253 Phylloxanthin, 90 Physalophrya, 745 spumosa, 741, 745 Physaridae, 430 Phy sella sp., 693 Physematiidae, 520 Physiological solution, 892 Physiology, 97-136 Physomonas, 360 Physophaga, 791 Phytia setifer, 778 Phytodiniidae, 325, 329 Phytodinium, 329 simplex, 828, 329 Phytomastigina, 6, 21, 23, 256-329, 881 884

heterochaeta, 534, rodericensis, 536

536-537

sermowaiana, 537 wendessiana, 536

Phialoides, 558 ornata, 556, 558

Phytomonadina, 256, 263, 276-290 Phytomonas, 353-354 davidi, 354 elmassiani, 354 Phytomyxinea, 433-434 Phytotrophic nutrition, 107-108 Pieris brassicae, 674
Pig, 9, 347, 349, 457, 460, 579, 586, 625, 639, 640, 799 Pigeon, 388, 583, 615, 619

Phialonema, 302
Philaster, 771


952
Pigments, 30, 31, 45,
Pileocephalus, 555 striatus, 553, 555
Pilisuctoridae, 753 Pimelia, 553 Pimephales notatus, 660

PROTOZOOLOGY
89-90

Plasmodium
falciparum,
floridense,

continued
15,

31,

32,

605,

606,

607, 609, 610, 613

618
602, 60S, 605,

gallinaceum,

616,

Pinaciophora, 513 fluviatilis, 512, 513 Pipetta, 522 tuba, 521 Piroplasma, 622 Pisania maculosa, 560 Pithiscus, 281 Pithothorax, 71-4
ovatus,

715

Pituophis, 377 Placobdella caienigera, 592 marginata, 352, 552, 588 Placocista, 489-490 spinosa, 489, 490
Placosilina, 499

cenomana, 498
Placopsilinidae, 499 Placus, 713 socialis, 711, 713

617 hexamerium, 616, 617 inconstans, 615 inui, 22 kochi, \2,614 knowlesi, 22, 33, 614 lophurae, 616, 617 hjgosomae, 618 malariae, 605, 607, 610-611, 613 mexicanum, 617-618 nucleophilum, 616, 617 oti, 616,617 ovale, 605, 607, 611-612 polare, 616, 617 praecox, 15, 615 rhadinurum, 618 relictum, 15, 600, 615, 616 rouxi, 615, 616 tenue, 610 vaughani, 615, 616
vivax, 32,

Plagiocampa, 712 marina, 711, 712 Plagiophrys, 480

parvipunctata, 4?8, 480 Plagiopyla, 27, 740 minuta, 741 nasuta, 740-741 Plagiopylidae, 737 Plagiopyxis, 484
callida, 484,

186-187, 599-600, 601

602, 603, 604, 605, 606, 607,

608-610, 613

Plasmodroma, 249, 254-679 Plasmogamy, 135 Plasmosome, 40 Plasmotomy, 135, 172-173

Plastin, 40

485

Platophrya, 865 Platycola, 859

longicollis, 858,

Plagiospira, 779 crinita, 778, 779 Plagiotricha, 834 Planaria, 859 limacina, 695
torva, ulvae,

859

Platydorina, 288 caudata, 288, 289 Platvhelminthes, 693, 694, 695, 696,
"767,

768
765

696 694

Platynematum, 764-765
sociale, 24, 764,

Planorhis corneus, 588 Planorbulina, 504 Planorbulinidae, 503

Plants,
5, 6,

Platyophrya, 712 lata, 711, 712

Platysporea, 649, 655-660 Platytheca, 344 microspora, S4S, 344 Plectoidae, 522 Pleodorina, 290
californica, 290 illinoisensis, 89, 289,

353, 354

Plasmagel, 46, 125

Plasmagene, 239

Plasmaiemma, 125, 126 Plasma-membrane, 46

Plasmasol, 46, 124, 125 Plasmodia, 427, 428 Plasmodiidae, 600-618

290

Pleurocoptes, 771
hydractiniae, 770, 771 Pleurocystis, 535
32, 39, 226,

Plasmodiophora, 433 brassicae, 433

Plasmodium,

7,

15, 30,

cuenoti, 535 Pleuromonas, 362

600-608, 889, 901 berghei, 614 brasiliarmm, 612, 614 catkemerium, 602, 60S, 625, 616 circumflexum, 616617 cynomolgi, 603, 604, 605, 612-613
elongatum, 602, 615-616

jaculans, 24, 362, 363

Pleuronema, 769
anodontae, 768, 769 coronatum, 24, 768, 769 crassum, 768, 769 jaculans, 24

marinum,

768,,

769


SUBJECT INDEX
Pleuronema
continued
setigerum, 768, 769 Pleuronematidae, 758, 769-771 Pleurostomata, 700, 723-728 Pleurotricha, 838 lanceolata, 887, 838 Plistophora, 676 kudoi, 676 longifilis, 668, 675, 676 Plodia inter punctella, 563 Plumatella fungosa, 670 repens, 670 Pocillomonas, 284 flos aquae, 282, 284 Podocyathus, 878 diadema, 877, 878 Podophrya, 868 collini, 868 elongata, 866, 868 fixa, 866, 868 Podophryidae, 863, 868-870 Poisonous substance, 99 Polar capsule, 76, 643 filament, 76, 643, 644 Polyblepharides, 284 singularis, 282, 284 Polyblepharididae, 276, 284 Polychaetes, 575, 576 Poly dor a caeca, 691 fiava, 691

953

Pomoxis sparoides, 31, 655, 660 Pompholyxophrys, 511 punicea, 511, 512 Pontigulasia, 484 vas, 484-485
Pontosphaera haeckeli, 266, 267 Porcellana platycheles, 867 Porifera, 861 Porochrysis, 260 aspergillus, 261 Porospora, 558 galloprovincialis, 558
gigantea, 558,

559

Porosporidae, 541, 558-560 Porotermes adamsoni, 392, 406, 410

grandis, 392 Portunus depurator, 573, 792, 848 Potamilla reniformis, 564 Potamoceros triqueter, 694 Potassium dichromate, 576 Poteriodendron, 342 petiolatum, 342 Pouchetia, 316 fusus, 315, 316 maxima, 315, 316 Pouchetiidae, 314, 316 Powdery scab, 434 Prairie dog, 579 Precystic stage, 447, 455 Preerythrocytic stage, 602 Prehensile tentacles, 60 Preparations, Microscopical, 890-901 Fresh, 890-894 Permanent, 894-901 blood film, 899-901 smear, 894-899 section, 901 Prepatent period, 602 Primite, 528, 612 Prismatospora, 554 evansi, 553, 554 Proactinomycin, 154 Proboscidiella, 379 kofoidi, 878, 379 Procavia brucei, 734 capensis, 734 Proceros, 694 Procryptotermes, 383 Proctodeal feeding, 404 Prodigiosin, 452 Proglyptotermes, 383 browni, 383 Proloculum, 494 Prolophomonas, 408 tocopola, 409 Promitosis, 145 Pronoctiluca, 314 tentaculatum, 314, 815 Pronoctilucidae, 314 Prorhinotermes simplex, 406 Prorocentridae, 312-313 Prorocentrinea, 312-313 Prorocentrum, 312

Polygastricha, 12 Polykrikidae, 314, 324 Polykrikos, 324

barneqateyisis, 324 kofoidi, 324, 325

Polymastigidae, 369, 376-377 Polymastigina, 70, 333, 369-397 Polymastix, 376

melolonthae, 376 Polymnia, 693 nebulosa, 575 Polymonadina, 369, 396-397 Polymorpha, 719 ampulla, 719 Polymorphina, 501 Polymorphinidae, 501 Polymyxa, 434 Poly plastron, 820

multivesiculatum, 70, 821 Polyploidy, 190

Polyrhabdina, 543 spionis, 542, 543

spinosus' bifurcata,' 543 Polysaprobic Protozoa, 23, 116

Polyspira, 75, 794 delagei, 793, 794 Polystomella, 501

Polystoma, 281
pascheri, 231,

232
281

uvella, 53, 231, 232, 280,

Polytomella. 283
agilis, 115, 282,

283

caeca,

283


954

PROTOZOOLOGY
Protozoa
continued
free-living,

Prorocentrum

continued micans, 312, 313 triangulatum, 312

discolor, 24, griseus, 713

20-28
of, 20,

Prorodon, 712

geographical distribution in thermal waters, 21

parasitic in

28

711,712-713

man,

see

Man,

teres,

72

Protozoa, 459,672,674, 694, 794, 852, 873

utahensis, 712

phylogeny

of,

249-253

Prorodonopsis, 720
coli,

719, 720

Prostomata, 700-720 Protanoplophrya, 694 stomata, 694, 695

Protective organellae, 70-76 Proteinase, 105, 106 Proteolytic enzyme, 106

physiology of, 97-136 reproduction of, 145-211 size of, 39, 109, 110 Protozoology in relation to biology, 6-7 cytology, 8 economic entomology, 7, evolution, 7, 8
genetics, 7

8,

10

Proteomyxa, 418-425 Proteromonas, 362 lacertae, 362, 363

Proterospongia, 341 haeckeli, 340, 341 Proterythropsis, 316
crassicaudata, 315, 316

geography, 8
geology, 8, 10 medicine, 8

phylogeny,

7,

Proteus, 437 Protista, 5 6, 12 T Protochrysis, 275

pisciculture, 9 sanitary science, 9 soil biology, 9-10

veterinary medicine, zoogeography, 8

Protrichocyst, 76

8,

phaeophycearum, 273, 275

Protociliata, 29, 459, 684,

685-688

Protocruzia, 804 pigerrima, 801, 804

Protomagalhaesia, 545 serpentula, 542, 545 Protomerite, 528 Protomite, 789

Protrichomonas, 377 legeri, 376, 377 Prowazekella, 362 Prowazekia, 362 Prunoidae, 521

Psammodromus

Protomonadina, 333, 339-365 Protomonas, 420 amyli, 420 Protomont, 789 Protoopalina, 688 intestinalis, 686, 688 mitotica, 686, 688 saturnalis, 686, 688 Protophrya, 776 ovicola, 775, 776 Protophyta vs Protozoa, 5
Protoplasm, 12 Protoplasmic movements, 101-102, 122-126 Protopsis, 316 ochrea, 315, 316 Protoradiophrya, 698 fissispiculata, 697, 698 Protospirura muris, 674 Protozoa, as non-cellular organisms, 5 as unicellular organisms, 5 coining of term, 11 colonial, 6, 47, 173-174
definition of,
5, 12 distinguished from Protophyta, 5 Metazoa, 6 ecology of, 20-35

hispanicus, 588 Psammoryctes barbatus, 663 Psammosphaera bowmanni, 47 fusca, 47

parva, 47
rustica, elegans, 620

47

Pseudemys

floridana mobilensis, 462

Pseudoblepharisma, 804 tenuis, 802, 804 Pseudoboa clelia, 458 Pseudocalanus elongatus, 324 Pseudochitinous substance, 47 Pseudochlamys, 479 patella, 478, 479

Pseudochromosomes, 166 Pseudochromulina, 258

asymmetrica, 258 pseudocyst, 529 Pseudodevescovina, 383-384
unifiagellata,

384

Pseudodifflugia, 487 gracilis, 485, 487 Pseudofolliculina, 808-809 arctica, 808, 809

Pseudogemma, 873
pachystyla, 873, 876

Pseudoklossia, 575
pectinis, 575 Pseudolynchia maura, 620 Pseudomallomonas, 258

fossil, 10,

493, 516

SUBJECT INDEX
Pseudomicrothorax, 739 agilis, 738, 739 Pseudopodia, 49-52, 97, 98, 99, 100, 417, 435 Pseudoprorodon, 713 farctus, 711, 713 Pseudospora, 420 eudorini, 420 parasitica, 420 volvocis, 419, 420 Pseudosporidae, 418, 420 Pseudotrichomonas, 390 keilini, 389, 390 Pseudotrichonympha, 413-414 grassii, 414 Pseudotrypanosoma, 391 giganteum, 391-392 Psilotricha, 834 acuminata, 838, 835 Pteridomonas, 335 pulex, 335, 336 Pterocephalus, 550 Pteromonas, 284 angulosa, 282, 284 Pterospora, 539 maldaneorum, 539, 540 Pterotracha coronata, 780 Ptychoptera contaminata, 555 Ptychostomum, 779 bacteriophilum, 778, 780 Pulsating vacuole, 83 Pusule, 108, 310 Pycnothricidae, 728, 733-735 Pycnothrix, 734 monocystoides, 734 Pyorrhoea alveolaris, 456 Pyramidochrysis, 260 modesta, 259, 260 Pyramidomonas, 282 Pyramimonas, 282 montana, 283 tetrarhynchus, 282 Pyrenoids, 89, 90 Pyrocystis, 329 Pyronin, 228 Pyrotheca, 676 incurvata, 676, 677
'

955
546

Pyxinioides, 546
balani,

Quadrula, 490 symmetrica, 489, 490

Quail, 336, 388, 393, 580, 582, 583,

620 Querquedula crecca, 620 discors, 620 Quinine, 600

R
Raabella, 782
botulae, 781, 782 Rabbit, 351, 374, 395, 457, 577 Races of Protozoa, 223-228 Rachidelus brazili, 459 Radial cytostomal fibrils, 68, 69 Radiating canals, 84

Radiolaria, 10, 12, 29, 39, 185, 249,

505, 516-524 Radiophrya, 696-697 hoplites, 697 Radium rays, 134 Rainey's corpuscles, 638 Raja, 655 oxyrhynchus, 353 Rana, 686 areolata, 687 cantabrigensis, 687 catesbeiana, 687 clamitans, 656 fusca, 377 pipiens, 656 palustris, 694 ridibunda perezi, 860 sphaenocephala, 656, 687 temporaria, 390 Ranatra linearis, 872 Raphidiophrys, 511 pallida, 511, 512

Raphidocystis, 511
infestans, 512 tubifera, 511-512

Pyrsonympha,
vertens, 379,

78, 79,

379

granulata, 379, 880

880

Python, 377 sebae, 459 Pyxicola, 858 affinis, 858

socialis, 858, 859 Pyxidicula, 478

Rat, 14, 351, 371, 374, 388, 395, 457, 579, 592, 614, 639, 641 Rattus norvegicus, 388 Reaction of Protozoa to Beta rays, 134 chemical stimuli, 132-133 current, 132
electrical stimuli,

135-136

gravity, 131-132

133-135 mechanical stimuli, 130-131 radium rays, 134

light,

operculata, 478 Pyxidium, 854

temperature, 135
ultraviolet rays, 133-134

urceolatum, 853, 854

vernale, 858,

854

Pyxinia, 557 bulbifera, 556, 557

X-rays, 134-135 Reconstruction band, 147, 148 Red snow, 21 tide, 311, 312
water, 311, 312, 313, 327, 706

956

PROTOZOOLOGY
Rhipidodendron, 358 splendidum, 359
Rhithrogena semicolorata, 676

Red-water fever, 622 Red-winged black bird, 615, 616 Reduction division, 160, 206-208, 234, 496, 573, 574, 575 Reduviid bugs, 349 Refringent body, 106-107, 440 Regeneration, 39, 55, 212-213 Reindeer, 822 Relation between neuromotor and silver-line systems, 67-69 nucleus and cytoplasm, 39-40, 212-213, 236-238 Remanella, 73, 88, 727-728 rugosa, 726, 728 Reophacidae, 497 Reophax, 498 nodulosus, 497
Reorganization band, 147, 148, 149 Reproduction in Protozoa, 145-211 asexual, 175-180 sexual, 180-211 Reptiles, 458, 583, 592, 625 Reserve food matter, 107, 112-115, 116 Reservoir hosts, 347, 349 Respiration, 82, 104, 116-118, 196 Retardation of movement, 891 Reticularia, 432 lycoperdon, 431 Reticulariidae, 432 Reticuliterrnes flaviceps, 405, 406, 412 flavipes, 379, 412, 674 hageni, 406, 410
hesperus, 379, 406, 410,

Rhizammina, 497 algaeformis, 497 Rhizamminidae, 497

Rhizobium sp., 443 Rhizocaryum, 691 concavum, 691, 692
Rhizochrysidina, 257, 267-269 Rhizochrysis, 267 scherffeli, 266, 267, 268
Rhizoflagellata, 685

Rhizomastigina, 333 Rhizomastix, 338 gracilis, 336, 338 Rhizoplasma, 422 kaiseri, 421, 422 Rhizoplast, 333 Rhizopoda, 12, 417-504 Rhizopodia, 49-50, 493 Rhizotrogus, 376, 557 Rhodomonas, 274 lens, 273, 274 Rhopalonia, 550 hispida, 550, 551 Rhopalophrya, 715
salina, 101, 102, 715,

716

Rhyncheta, 876
cyclopum, 876, 877 Rhynchobolus americanus, 543 Rhynchocystidae, 531, 534 Rhynchocystis, 534
pilosa, 534, 585 porrecta, 534, 535

412
lucifugus, 405, 412, 674 speratus, 405, 412, 414
tibialis, 412 Reticulomyxa, 423-424 filosa, 424-425 Retortamonas, 362-363 blattae, 363 caviae, 364 gryllotalpae, 363 intestinalis, 363-364, 885 Rhabdammina, 497 abyssorum, 497 Rhabdocystis, 533 claviformis, 532, 533 Rhabdomonas, 303

Rhynchogromia, 472 Rhynchomonas, 362

marina, 362
nasuta, 23, 24, 362, 363

Rhvnchonympha, 411
tarda, 411,

413

Rhynchophrya, 875
palpans, 875, 876 Ribose nucleic acid, 44, 150

Ringer-egg media, 887-888 Ringer's solution, 887-888, 891

Ringform

in

Plasmodium, 601, 608

Robins, 615

Rontgen Rays on Protozoa, 134-135 Root hernia, 433

Rostellum, 374, 378, 379 Rostronympha, 407

incurva, 54, 170, 171

Rhabdophrya, 866-867
trimorpha, 866, 867 Rhabdostyla, 854 vernalis, 853, 854 Rhagadostoma, 712 Rhaphiceros, 822 Rhaphidomonas, 306 Rhesus, 456 Rhinoceros unicornis, 824, 826 Rhipicephalus appendiculatus, 625
evertsi,

magna, 407, 408 Rotalia, 502

beccarii,

501

Rotaliidae, 502 Rotifera, 637, 638

625

sanguineus, 624

Rotundula, 547 gammari, 547, 549 Rugitermes, 383 Rupertia, 504 stabilis, 503 Rupertiidae, 504 Ruppia, 418, 434


SUBJECT INDEX
Schellackia

957
continued

Saccammina, 497 sphaerica, 497 Saccamminidae, 497

Saccinobaculus, 70, 379 amploaxostylus, 380 Sagartia leucolena, 789 parasitica, 763 Sagenoscene, 523
Sagitta, 692 claparedei, 466 Sagosphaeridae, 523 Salamander, 694 Salientia, 685 Salinity vs Protozoa, 24-25

perciciosa, 588 Schizamoeba, 34, 463-464 salmonis, 464, 465 Schizocystidae, 560, 562-565 Schizocystis, 562 gregarinoides, 561, 562-563 Schizogony, 175, 526, 560, 599, 601 erythrocytic, 599, 601, 608, 609 exoerythrocytic, 602-605 Schizogregarinina, 527, 560-565 Schizont, 175, 599, 601, 609 Schizotrypanum cruzi, 348 Schneideria, 557 mucronata, 556, 557

Salmo

gairdneri, 650 irideus, 372

Schuffner's dots, 605, 608, 611

Schultzella, 476 diffluens, 474< 476 Schultzellina, 696 mucronata, 696, 697

14, 393, 649 Salmonella, 799

Salmon,

Salmonid fish, 464, 649, 658 Salpa, 321 Salpa mucronata-democratica, 785
Salphvoeca, 341
fusifnrmis, 341, 342 Salvelinus fontinalis, 372 Sand flies, 355, 691, 7c 3

Sciadiophora, 556
phalangii, 556 Sciadostoma, 739 Sclerotia, 427, 428
Scololepis fuligi?wsa, 543, 565

Scolopendra, 550
cingulata, 550, 590
heros,

Sapotaceae, 353 Sappinia, 443 diploidea, 443 Saprodinium, 829 dentatum, 829, 830 putrinum, 829, 830 Sapropelic Protozoa, 23 Saprophilus, 765 agitatus, 764, 765 muscorum, 764, 765 Saprophytic nutrition, 108- 100 Saprozoic nutrition, 89 Sarcina flava, 115 Sarcocystis, 639 bertrami, 641 lindemanni, 639-640
miescheriana, 638, 640-641 muris, 641 rileyi, 639, 641 tenella, 638, 639, 640 Sarcode, 12 Sarcodina, 10, 42, 249, 250, 254, 417-

557

subspinipes, 550 Scoloplos nmlleri, 636

Scourfieldia, 279

complanata, 278, 279

Scutigera, 550
forceps, 550

Scyphidia, 852 amphibiarum, 851, 852 Scyphidiidae, 850, 852

Scytomonas, 303
pusilla, 24, 302, 303 Secondary nucleus, 417, 465 Secretion, 118-122 Section preparation, 901 Selective power of Protozoa, 47

Selenidium, 563
potamillae, 563-564 Selenococcidiidae, 571, 572

Selenococcidium, 572 intermedium, bl2

Selenocystis, 564-565
foliata,

525 Sarcophaga, 354

Sarcosporidia, 14, 638-641 Sardine, 584

565
196,

528 Scaphiopus albus, 688

Satellite,
solitarius,

Senescence, 208-211 Sensitive race in Paramecium, 236, 238-241

688 618

Sensomotor apparatus, 68 Sepia, 694

officialis,

Sceloporus ferrariperezi, 617-618

olivaceous,

573

undulatus, 618 Schaudinnella, 538 henleae, 537, 538 Schaudinnellidae, 531, 537-538 Schellackia, 588
bolivari,

Sepiola rondeletii, 694 Sericostoma, 555 Serinus canaria, 615 Serotypes, 242
Sessilia,

850-859

588

Seticephalus, 550 clegans, 550, 551

95S

PROTOZOOLOGY
Soil Protozoa, 9, 28, 423, 443,

Sewage organisms, 23
Sex factors, 233
reaction types, 192-197 substance, 181, 196, 197, 235 Sex-linked inheritance, 233 Sexual fusion, 180-187, 599, 601, 685 Sexual reproduction, 29

472

Solanum, 434
Solea vulgaris, 591

Solenophrya, 873 inclusa, 872, 873 pera, 872, 873

Solutions, Chalkley's, 882

amphimixis, 203 autogamy, 203-204 automyxis, 203 conjugation, 187-203 Cytogamy, 204 paedogamy, 204-205 sexual fusion, 180-187, 599, 601, 606-607 syngamy, 180-187 Sheep, 350, 375, 457, 577, 578, 625,
640, 751, 817, 818, 819, 820, 821,

Hahnert's, 882-883 Locke's, 887 Lugol's, 892 Pace and Belda's, 883 Ringer's, 887-888, 891
Saline,

892

Sonderia, 741-742 pharyngea, 741, 742

vorax, 741, 742 Sorodiscus, 434 Sorophora, 430, 433

822
Shell, 10, 47-48, 70, Sialia s. sialia, 617 Sieboldiellina, 695
Silica,

472

planariarum, 695-696 47-48, 493

Silicina, 497 limitata, 497 Silicinidae, 497 Silicofiagellidae, 257, 267 Silkworm, 10, 14, 670, 671 Silpha laevigata, 555

Sorosphaera, 434 Spadella bipunctata, 466 inflata, 466 serratodentata, 466 Sparrow, 351, 586, 615 Spasmostoma, 710 viride,^ 710, 711 Spathidiella, 701 Spathidiidae, 700-703 Spathidioides, 701
sulcata,

701-702

thoracica,

554

Spathidiopsis, 713

Silver-impregnation method, 66 Silver line, 66, 67 Silverline system, 66, 67, 68

Spathidium, 700
spathula, 72, 700, 701

Simulium, 668 parnassum, 622 venustum, 620 Sinuolinea, 654 dimorpha, 652, 654 Siphonophora, 321, 357 Siphostoma, 656
Sipunculoida, 661 Sipunculus, 538 nudus, 539 Size difference, 109-110, 111 Skeleton, 47-48, 417, 517 Skink, 618

Spermatozopsis, 283 exultans, 282, 283 Sphaenochloris, 280 printzi, 280

Skunk, 579
Slavina appendiculata, 590, 676 Sleeping sickness, 15, 30

Gambian, 30, 347 Rhodesian, 348

Slides, microscopic,

890

Sphaeractinomyxon, 661-662 gigas, 662, 663 stolci, 662 Sphaerastrum, 510 fockei, 509, 510 Sphaerella, 277 Sphaerellopsis, 277 fluviatilis, 277 Sphaerium, 769 corneum, 693, 783, 784 rivicola, 783 Sphaerita, 45, 893 Sphaerocapsa, 520 Sphaerocapsidae, 520 Sphaerocystis, 548 simplex, 548
Sphaeroeca, 341 volvox, 840, 341 Sphaeroidae, 521 Sphaeromyxa, 656
balbianii, 172, 656, 657 sabrazesi, 187, 645-648, 656-657 Sphaerophrya, 868 magna, 868 soliformis, 868, 869 stentoris, 868

Slime molds, 427 Slugs, 388, 747, 760

Smear preparations, 894-901

Smelt, 668 Snails, 357, 588, 590 Snake, 351, 377, 458-459, 584 Snyderella, 397 tabogae, 896, 397 Sodium chloride on nucleus, 42 Protozoa, 24-25

SUBJECT INDEX
Sphaerorhynchus, 552 ophioides, 553 Sphaerospora, 653 pernicialis, 654 pohjmorpha, 35, 652, 653, 654, 672 tincae, 652, 654 Sphaerosporea, 649, 651-655 Sphaerosporidae, 65 1, 653-654 Sphaerozoidae, 522 Sphaerozoum, 522 ovodimare, 521 Sphaleromantis, 260 ochracea, 259, 260 Sphenoderia, 490 lenta, 489, 490 Sphenophrya, 785-786 dosiniae, 786 Sphenophryidae, 774, 785-787 Spheroid colony, 174, 286, 289 Spider monkey, 735
Spindle
fibers, 155, 157, 158, 161, 163,

959

164
Spionidae, 543 Spiraulax, 327 jolliffei, 327, 828 Spireme ball, 199
Sprillina, 502 vivipara, 494, 495 Spirillum volutans, 114, 115

Spirotrichonympha, 406 bispira, 406 leidyi, 405, 406 pulchella, 405, 406 Spirotrichonymphella, 406 pudibunda, 406 Spirotrichosoma, 406-407 capitata, 407 Spirozona, 740 caudata, 738, 740 Spirozonidae, 737, 740 Spirula, 694 Spleen index, 30 Spondylomorum, 288 quaternarium, 288, 289 Sponge, 861 Spongilla fluviatilis, 861 Spongomonas, 358 uvella, 358, 359 Spongospora, 434 Sporadin, 528 Sporangium, 428
Spore, 180, 526, 635, 638, 639, 643

Spirobolus spinigerus, 544

Spirobutschliella,
chattoni,

693-694

actinomyxidian, 660-661 cnidosporidian, 643 haplosporidian, 635, 637 helicosporidian, 678, 679 microsporidian, 180, 668-669, 677 mycetozoan, 429 myxosporidian, 643-644 Spore membrane, 526, 643
Sporoblast, 571 Sporocytes, 645 Sporogony, 526, 645 Sporokinete, 623, 624 Sporont, 623, 643, 645, 669 monosporoblastic, 645
disporoblastic, 645 Sporophore, 429 Sporoplasm, 643, 644 Sporozoa, 14, 30, 179, 249, 250, 254,

694

Spirochona, 847

gemmipara, 847, 848 Spirochonidae, 847-848 Spirocystis, 562 nidula, 562 Spirodinium, 824 equi, 823, 824 Spiroglugea, 678 octospora, 677, 678 Spirogonium, 283 chlorogonioides, 282, 283 Spirogyra, 420 Spiroloculina, 499 limbata, 498 Spiromonas, 359 augusta, 359 Spironympha, 406 Spirophrya, 789-790
sabparasitica, 790, 791 Spirorhynchus, 800 verrucosus, 800, 801 Spirostomidae, 796, 801-806

526-682
Sporozoite, 187, 526, 527, 571, 599, 600, 601 607 Sprat, 584
,

Squalorophrya, 875 macrostyla, 874, 875

Squirrel, 349, 389, 457, 579 Stains, 896-899, 900-901 Delafield's, 78, 897 Feulgen's nucleal reaction,

897-

898
Fontana's, 899 Giemsa's, 897, 900 Heidenhain's, 896-897 Mallory's, 63, 78 Mayer's, 897 Silver-impregnation, 898 Vital, 891 Wright's, 901 Stalk, 76
Starfish, 32 Starling, 615

Spirostomum, ambiguum,

27, 116, 801-802 22, 25, 27. 108,

117,

802, 803 filum, 802, 803 intermedium, 802, 803 loxodes, 802, 803 minus, 24, 802, 803 teres, 24, 802, 803
Spirotricha, 690,

796-846

960

PROTOZOOLOGY
Stigmatogaster gracilis, 550 Stokesia, 767 vernalis, 766, 767
Stokesiella, 360 dissimilis, 360, 861 leptostoma, 360, 861 Stolotermes victoriensis, 407

Starvation on Protozoa, 115-116

Stasziecella, 314 Statocyst, 87, 88 Statolith, 87, 88

Staurocyclia, 522 phacostaurus, 521 Staurojoenina, 412

assimilis,
Jf.ll,

412

Staurojoeninidae, 404, 412

Staurophrya, 867 elegans, 866, 867 Steenbok, 822 Steinella, 694 uncinata, 694 Steinia, 832 Steinina, 555 rotunda, 558, 555 Stelexomonas, 342-343 dichotoma, 343 Stemonitidae, 431 Stemonitis, 431
splendens, 480 Stempellia, 674 magna, 668, 669, 674, 675 Stenopelmatus fuscus, 545
pictus, 545 Stenophagous Protozoa, 27 Stenophora, 544 larvata, 542, 544 robusta, 542, 544 Stenophoridae, 541, 544 Stenostomum leucops, 693 Stentor, 11, 39, 79, 806 amethystinus, 29, 807

Stomatophora, 536 coronata, 585, 536 Stomatophoridae, 531, 536-537 Stomatostyle, 750 Strains of Protozoa, 223-228, 607 Streblomastigidae, 369, 374 Streblomastix, 374 strix, 154, 374 Streptomonas, 359 cordata, 359 Streptomycin, 889 Strobilidiidae, 814, 815-816 Strobilidium, 815-816 gyrans, 815, 816 Strombidinopsis, 816 gyrans, 815, 816 Strombidium, 814 calkinsi, 814 815 Strongylidium, 836 californicum, 835, 836
Strongylocentrotus franciscanus, 741 droebachiensis, 741, 749, 750
lividus,

762

purpuratus, 741, 748

coeruleus, 22, 27, 28, 45, 61,

148,

805, 806 igneus, 805, 807 mulleri, 805, 806-807 multiformis, 807
niger,

Sturnus v. vulgaris, 615 Stylobryon, 360 abbotti, 360, 361 Stylocephalidae, 541, 552-553 Stylocephalus, 552
giganlens, 552,

558

Stylochona, 847

807 polymorphus, 805, 806 pyriformis, 807 roeseli, 805, 807 striatus, 806

848 Stylochromonas, 262 minuta, 262

coronata, 847,

Stylochrysalis, 263
parasitica, 263 Stylocometes, 867
digitatus,

Stentoridae, 796, 806-807 Stentorin, 45, 81

867

Stephanonympha, 397
nelumbium, 396, 397 Stephanoon, 287-288 askenasii, 288, 289 Stephanopogon, 712 colpoda, 711, 712 Stephanosphaera, 289 pulvialis, 183, 185, 289 Stephoidae, 522
Stichopus califor nicus, 811
Stichotricha, 836 intermedia, 835, 836 secunda, 885, 836 Sticklebacks, 672 Stictospora, 557 provincialis, 556, 557

Stylocystis, 555 praecox, 553, 555 Stylonychia, 11, 23, 24, 44, 839 mytilus, 839, 840 notophora, 839, 840 pustulata, 27, 148, 208, 209, 839,

840
putrina, 839, 840

Stylophrya, 867 Stylopyxis, 266

mucicola, 264, 266 Styloscolex, 697, 698

Snbneucleus, 153
Succinia, 590
putris,

776

Stigma, 89, 90-91

Succinic dehydrogenase, 106 Sucker, 76, 85

SUBJECT INDEX
Suctoria, 12, 28, 44, 249, 683,

961

863-

878
Suctorial tentacle, 60 Sudan III and IV, 105, 114, 892 Sulcoarcus, 720 pellucidulus, 719, 720 Sulcus, 310 Sun animalcules, 507 Supportive organellae, 70-76 Surface tension, 122, 124 Surra, 350 Sutural plane, 643 Swarmers, 518, 519 Sycia, 543 inspinata, 542, 543
Syllis gracilis, 637 Symbiosis, 29, 105,

Tarentola, 362 Teal, blue-winged, 620 Teal duck, 620 Tectin, 47 Tegula brunnae, 784 Teleuscolex, 697, 698 Tellina, 576, 779 balthica, 776 Telomyxa, 678 glugeiformis, 677, 678 Telomyxidae, 678 Telosporidia, 526-634 Telotroch, 850 Temperature and Protozoa, 20-22,
134, 196, 204, 239, 242, 456, 579,

607
107, 108,
121,

241, 369, 440

Symmetry, 39
bilateral, 39, 392, radial, 39

Tenebrio molitor, 545, 561 Tentacles, 59-60, 99, 707, 708, 863 Tentaculifera, 727, 863

394

Teranympha, 414 Teratonympha, 414

mirabilis, 411, 414 Teratonymphidae, 405, 414

universal, 39

Sympetrum rubicundulum, 554

Synactinomyxon, 663
'

tubificis,

662, 663

Synapta, 538 Synchaeta, 637 Syncrypta, 262 volvox, 262, 263

Syncriptidae, 257, 262-263 Syncystis, 563 mirabilis, 563, 564 Syndiriium, 323-324 turbo, 322, 324

Teredo, 779 navalis, 779 Termite Protozoa, 29, 105, 543, 545,
674, 885-886 Termones, 181 Termopsis anguslicollis, 374 Test, 47-48, 472, 493 Testacea, 169, 418, 472-490, 883 Testudo argentina, 458 calcarata, 458 graeca, 458 Tetrablepharis, 283 multifilis, 282, 283 Tetractinomyxidae, 661 Tetractinomyxon, 661 intermedium, 661, 662 Tetradimorpha, 335 radiata, 335, 336 Tetrahymena, 760, 884 geleii, 760 limacis, 760

Syngamy, 180
Synkaryon, 183 Synophrya, 792
hypertrophica, 791, 792

Synura, 262 adainsi, 263 uvella, 262-263 Synuropsis, 262 Syphacia obvelata, 390 Syringopharynx, 780 pterotrachae, 780 Systenus, 550, 563 Systole, 83 Syzygy, 528, 530

piriformis, 26, 34, 225, 227, 759, 760, 761 vorax, 26, 109, 110, 227, 760

Tetramastix, 374 Tetramitidae, 369, 371-374 Tetramitus, 371

pyriformis, 371, 373
rostratus, 21, 60, 371, 372, salinus, 371, 373

Tachyblaston, 873
ephelolensis, 872,

873

373

Tachysoma, 832-833
parvistyla, 833 Tactile organelles, 57

Tetramyxa, 434 Tetrataxis, 499

palaeolrochus, 498 Tetratoxum, 824 escavatum, 824 parvum, 824

Taeniocystis, 557 mira, 556, 557

Taliaferria, 735 clarki, 734, 735 Talorchestia longicornis, 733

Tanypus, 555 Tapes aureus, 787 Tapioca disease, 649

unifasciculatum, 823, 824 Tettigonospora, 545

stenopelmati, 545 Teutophrys, 703


962

PROTOZOOLOGY
continued
Tiliqua scincoides, 458

Teutophrys
Texas

trisula, 703, 704 fever, 14, 622

Tinea

tinea,

654

Textularia, 498 agglutinans, 498 Textulariidae, 498 Thalassema neptuni, 552, 572 Thalassicolla, 520
nucleata, 521 Thalassicollidae, 520

Tintinnidae, 48, 814, 816 Tintinnidium, 816 fluviatile, 815, 816 semiciliatum, 815, 816 Tintinnopsis, 63, 816
cylindrata, 815, 816 illinoisensis, 815, 816

Thalassophysa, 521 Thalassophysidae, 520 Thalassothamnidae, 521 Thalassothamnus, 521 Thamnomys surdaster, 614 Thaumatomastix, 307 setifera, 307 Thaumatophrya, 875 trold, 875, 876 Thecacineta, 870 cothtirnioides, 871, 872 gracilis, 871, 872 Thecamoeba, 472

Tipula, 338, 376, 459 abdominalis, 592 Toad, 335, 374, 390, 651, 655, 656,
686, 687, 688, 860 Toadfish, 35, 653, 672

Tokophrya, 870
cyclopum, 172, 870, 871 infusionum, 870, 871 Tomite, 752, 753, 789, 790 Tomont, 789, 790 Tontonia, 815 gracillima, 815 Torodinium, 320 robustum, 819, 320 Torpedo, 655 Torquenympha, 410 octoplus, 409, 410 Toxicyst, 73 Toxoglugea, 678 gerridis, 677, 678 vibrio, 677, 678 Toxonema, 678 Toxoplasma, 603, 625 gondii, 625-626 Toxoplasmosis, 626 Tracheliidae, 723, 725-727 Trachelius, 725 ovum, 725, 726 Trachelocerca, 717 phoenicopterus, 716, 717 subviridis, 716, 717 Trachelomonas, 58, 299 hispida, 89, 299, 800 piscatoris, 299, 800 urceolata, 299, 800 vermiculosa, 300 verrucosa, 300 Trachelophyllum, 716 clavatum, 715, 716 Trager's media, 885 Tramea lacerta, 554 Transverse flagellum, 310 Traumatiophtora, 794 punctata, 793, 794 Tremalith, 266 Trematodes, 393, 637 Trentonia, 307 flagellata, 307 Trepomonas, 395 agilis, 23, 24, 392, 395
rotans,

Thecoplasm, 61 Theileria, 625 parva, 624, 625 Thelohanellus, 660

notatus, 31, 154, 659, 660

Thelohania, 674 illinoisensis, 674

180, 674, 675 multispora, 668 opacita, 8, 668, 674, 675 reniformis, 674, 675 Theobaldia, 606, 615, 617 annulata, 34
legeri, 7,

Thermal waters and Protozoa, 21

Thermobia domestica, 548 Thigmophrya, 776 macomae, 776 Thigmophryidae, 774, 776 Thigmotricha, 29, 690, 774-787 Thoracophrya, 713 Thorakomonas, 279
sabulosa, 278, 279 Thuricola, 857
folliculata, 24,
kellicoltiana,

858

Thuricolopsis, 858

858 Thylacidium, 798 truncatum, 797, 798 Thylacomonas, 343-344 compressa, 848, 344

Thymonucleic
Tiarella, 779

acid, 42, 148,

898

Thyrsites atan, 655

Tiarina, 707 fusus, 707 Ticks, 349, 353, 592, 622, 624, 625
Tillina, 747 canalifera, 81, 746, 747 helia, 762 magna, 24, 178, 746, 747

892,395

Triactinomyxidae, 661-663 Triactinomyxon, 661 dubium, 661

SUBJECT INDEX
963
continued

Triactinomyxon continued
ignotum, 661, 662 legeri, 66 magnum, 661 mrazeki, 661 Triadinium, 824 caudatum, 823, 824
galea, 824 minimum, 823, 824 Triangulomonas, 306 rigida, 305, 306 Triatoma, 349 dimidiata, 349, 565 gerstaeckeri, 349 heidemanni, 349 longipes, 349 megista, 349 protracta, 349 rufo'da, 349 Tricaudalia, 824 Tricercomitus, 390 termopsidis, 390-391, 886 Tricercomonas, 372 intestinalis, 373 Trichia, 432 affinis, 431 Trichiidae, 432 Trichite, 71, 72, 74 Trichitosome, 74 Trichlorididae, 276, 281 Trichloris, 281 paradoxa, 280, 281 Trichocera annulata, 463 hiemalis, 463 regelationis, 463 Trichochona, 847 lecithoides, 847, S^S

Trichonympha
collaris,

campanula, 100, 156, 412, ffS, 886 886 grandis, 413 sphaerica, 886 Trichonymphidae, 405, 412-414 Trichopelma, 739 sphagnetrum, 738, 739 Trichopelmidae, 737, 739 Trichophrya, 865 columhiae, 864, 865 epistylidis, 864, 865 salparum, 864, 865 sinuosa, 865 micropteri, 864, 865 Trichorhynchus, 550, 739
pulcher, 550, 551 Trichospira, 740 inversa, 738, 740 Trichospiridae, 737, 740 Trichostomata, 690, 737-754 Trichotaxis, 838 stagnatilis, 837, 838 Trichuris, 463

Trigonomonas, 395 compressa, 392, 396 Triloculina, 499 trigonula, 498

Trilospora, 651
californica,

651

Trimastigamoeba, 436 philippinensis, 436 Trimastigidae, 369, 370-371 Trimastix, 370

convexa, 370, 391

marina, 370

Trimyema, 739-740
compressum, 24, 755, 740

Trichocyst, 11, 71-76, 102, 273, 793 Trichocystosome, 74, 75 Trichodina, 859
pediculus, 859, 860 ranae, 860
sp.,

Trimyemidae, 737, 737-740 Trinema, 489

enchelys, 28, 489

860

linear e, 182, 183, 489 Triodopsis albolabris, 357

tridentata,

urinicola,

859-860

357

Trichoduboscqia, 676 epeori, 675, 676 Trichomastix, 376

Trionyx indicus, 620

Tripalmaria, 824
dogieli, 824, S5 Triplagia, 522 primordialis, 522

Trichomonadidae, 370, 385-392 Trichomonadina, 385 Trichomonas, 13, 14, 55, 385, 886 buccalis, 386 columbae, 388 elongata, 386
gallinae, 227, 387,

388

hominis, 385-386, 387, 388, 885

limacis,

388 388

linearis, 387,

macacovaginae, 388

388 tertax, 386, 387, 885 vaginalis, 26, 386-387, 885 Trichonympha, 184, 186, 412
microti, 387,
agilis, 412, 4-7S

Triplumaria, 824 hamertoni, 824, 826 Tripneustes esculentus, 750, 771 Tripylea, 519, 523-524 Triticum, 434 Triton, 852 taeniatus, 377 Tritrichomonas, 388 augusta, 389, 390 batrachorum, 389, 390
brevicollis, 389,

390

caviae, 390 fecalis, 34, 388-389 /oeiws, 388, 389


904
Tritrichomonas continued muris, 389-390 Triturus, 859 viridescens, 352 Trochammina, 499 inflata, 498 Trochamminidae, 499 Trochila, 730 palustris, 729, 730 Trochilioides, 730 recta, 24, 729, 730 Trochocochlea articulata, 560
mutabilis, 558, 560 turbinata, 560

PROTOZOOLOGY
Trypanosomatidae, 339, 344-357 Trypanosomiasis, 345 Trypsin-like enzymes, 106, 345, 347, 348, 349 Tsetse flies, 14, 345, 347, 348 Tubifex, 538 inflatus, 696 ta&tfex, 661, 663, 676 Tubulina, 432
fragiformis, 481 Tubulinidae, 432 Tunicate, 321, 674, 865

Trochodinium, 320
prismaticum, 319, 320 Troglodytella, 63, 826 abrassarti, 825, 826
var. acuminata, 826

Turbellaria, 768 T urdus m. migratorius, 615 Turkey, 336, 375, 388, 393, 583, 854 Turtle, 351, 458, 462, 583, 592, 620, 874, 875

826 Trophochromatin, 414 Trophocyte, 321 Trophonia plumosa, 576 Trophont, 752, 753, 789 Trophozoite, 175 Tropidoscyphus, 304 octocostatus, 304, 805 Trout, 393 Trutta fario, 393 Trypanodinium, 323 ovicola, 322, 323 Trypanoplasma, 357
gorillae,

Tuscarora, 524 murrayi, 524 Tuscaroridae, 524

Tussetia, 281, 345 Twist disease, 649, 658

Typhlogobius calif'or niensis, 651 Tyzzeria, 588

U
Uca
pugilator, 543

pugnax, 543
Ulivina, 543 rhynchoboli, 543 Ultraviolet rays, 133-134

Trypanosoma,

8, 13, 32, 55, 56,

344-

345, 886, 901 americanum, 350 brucei, 14, 228, 349-350 cruzi, 30, 227, 348-349, 886 danilewskyi, 852, 353 diemyctyli, 352 duttoni, 351 equinum, 55, 350 equiperdum, 350, 351 ewon, 54, 55, 230, 350

Undulating membrane, 345 Unicapsula, 652

55, 56, 58, 59,

muscularis, 204, 648, 652, 658 Unicapsulidae, 651, 652

Unicauda, 660
clavicauda, 659, 660 Uradiophora, 545-546 cuenoti, 546, 549 Urceolaria, 859 karyolobia, 859 mitra, 859, 860 paradoxa, 859, 860 Urceolariidae, 859-861 Urceolus, 302 cyclostomus, 302 sabulosus, 302 Urea, 120 Urechis caupo, 543 Urinympha, 411-412 talea, 411, 412 Urnula, 869-870 epistylidis, 869, 870 Urocentrum, 765-766 turbo, 766 Uroglena, 265 volvox, 264, 265 Uroglenopsis, 265 americana, 264, 265 europaea, 265 Uroleptopsis, 835 citrina, 885, 836

gambiense, 15, 21, 30, 345-347, 880 giganteum, 352, 353 granulosum, 352, 353

hippicum, 351 inopinatum, 352

-

feu* **,

14,

32, 54,

117, 226, S^tf,

350, 351

melophagium, 350 nabiasi, 351 neotomae, 351 noctuae, 351 paddae, 351 percae, 352, 353 peromysci, 351 raj'ae, S5#, 353 remaki, 352, 353
rhodesiense, 347, 348, 886 rotatorium, 55, 352
theileri,

350

triatomae, 351

SUBJECT INDEX
Uroleptus, 834
halseyi, 149, 835 limnetis, 834, 835

905

Vectors, 347, 349, 356, 357, 606-607

longicaudatus 835
,

mobilis, 209, 228,

229

Uronema, 767 marinum, 24,

Uronychia, 843
setigera, 842,

766, 767 pluricaudatum, 766, 767

843

Urophagus, 396
rostratus, 892,

Vegetative stage, 175 Ventral cirri, 58 Ventral motor strand, 63 Venus fasciata, 779 ovata, 786 Verneuilina, 499 propinqua, 498 Verneuilinidae, 498 Veronica, 434 Vertebralina, 499
striata,

396

498

Urosoma, 833
caudata, 833

Urospora, 538
chiridotae, 537,

Vesicular nucleus, 40-42 Viability of cysts, 177, 450-453, 748 Viperia aspis, 587

538

hardyi, 539 Urosporidae, 531, 538-540 Urosporidium, 636 fuliginosum, 637 Urostyla, 44, 836

Virus, 241 Vital stains, 891

Vitamins, 112
Vitrina, 590 Viviparus fascialus, 784

caudata, 836, 837

coei,

837

grandis, 148, .70,5, 166, 535, 836 polymicronucleata, 837

trichogaster, 835,

836

Urotrichia, 710 agilis, 710, 7/i /arcta, 710, ?7J

labiata, 712 parvula, 710 Urozona, 766
biltschlii,

766, 767

Utricaceae, 353

Vacuolaria, 306 virtscens, 306, 307 Vacuome, 79 Vaginicola, 857 annulata, 857, 555
leptostoma, 857, 555 Vaginicolidae, 857-859

japonicus, 694 malleatus, 694, 784 Vole, 614 Volutin, 45, 114-115 Volvocidae, 276, 285-290 Volvox, 11, 39, 420, 2 85 aureus, 181, 285, 286 chaos, 11 globator, 285, 286 perglobator, 286, 287 spermatosphaera, 286, 287 tertius, 285, 287 weismannia, 286, 287 Vorticella, 11, 23, 79, 103, 855-856 campanula, 855, 856 convallaria, 855, 856 microstoma, 199, 200, 855, 856 monilata, 46, 855, 856
nebulifera, 199 picta, 855, 856 Vorticellidae, 850,

855-857

W
Wagnerella, 512-513 borealis, 512, 513 Wardia, 651
ovinocua, 651, 652

Vahlkampfia, 34, 442 fe'max, 21, 442 patuxent, 441, 442 Valvulina, 499 triangularis, 498 Valvulinidae, 499 Vampyrella, 420 lateritia, 119, 419, 420 Vampyrellidae, 418, 420-425 Vampyrophrya, 794 pelagica, 792, 793, 794 Varanus salvator, 458 varius, 458
Variation in Protozoa,
7,

Wardiidae, 649, 651 Wenyonella, 584 africana, 584

gallinae, 584-585 Whelk, 574 Woloszynskia, 328 Woodchuck, 580 Wood rat, 349

Woodroach,

109-H0,

223-243 Vasicola, 703

ciliata, 703,

29, 105, 378, 379, 380, 393, 407, 409, 410, 411, 412, 413, 414, 810

Woodruffia, 748

704

metabolica, 748
rostrata, 746,

grandis, 703

748

Vaucheria, 418

Wormy

halibut, 648, 652, 653

966

PROTOZOOLOGY
Zoomastigina, 23, 256, 333-414, 884886 Zoopurpurin, 46, 81 Zootermopsis anguslicollis, 377, 390, 412, 543, 545 laticeps, 391, 412
nevadensis, 377, 412, 543, 545

X-irradiation, 197, 239

Xanthophyll, 90, 306 Xenotis megalotis, 655 Xiphocaridina compressa, 794

Xylophagous Protozoa, 369, 378, 381,

404

391,

Y
Yatren, 452 Yeast, 443, 639

Zoothamnium,

39, 62,

857

Yellow throat, 617

Zannichellia, 418, 434

Zelleriella, 8, 688 antilliensis, 688 elliptica, 166, 687,

688

hirsuta,

688

scaphiopodos, 688

Zonomyxa, 481
violacea,

481

Zooamylon, 112, 528

Zoochlorellae, 29, 108, 507, 703, 739, 744, 767, 770, 806, 807, 814, 815,

834

adamsi, 856, 857 arbuscula, 856, 857 Zootrophic nutrition, 88, 97-107 Zooxanthellae, 29, 108, 274, 517, 844 Zostera, 418 marina, 418 Zschokkella, 657 hildae, 657 Zygocystidae, 531, 534-535 Zygocystis, 534 wenrichi, 534, 535 Zygosoma, 543 globosum, 542, 543 Zygote, 182, 183, 186, 529, 571, 599, 601 Zyrphaea crispata, 782

This Book

PROTOZOOLOGY
(Fourth Edition)

By Richard

R. Kudo, D.Sc.

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