ELSEVIER

Review of Palaeobotany and Palynology 105 (1999) 201235

Morphology and ultrastructure of elater-bearing pollen from

the Albian to Cenomanian of Brazil and Ecuador:
implications for botanical affinity
Rodolfo Dino a,b, , David T. Pocknall c , Mary E. Dettmann d
a

Petrobras, Cenpes-Divex-Sebipe, Cid. Univ., Ilha do Fundao, 21949-900 Rio de Janeiro, Brazil
b UERJ, Univ. do Estado do Rio de Janeiro, 20550-013 Rio de Janeiro, Brazil
c Amoco Corporation, Exploration and Production Technology Group, PO Box 3092, Houston, TX 77253, USA
d Department of Botany, University of Queensland, Brisbane, Qld. 4072, Australia
Received 27 April 1998; revised version received 28 September 1998; accepted 23 October 1998

Abstract
The morphological range of elaterate pollen grains is reassessed on the basis of detailed light, scanning electron
and transmission electron microscope analyses of representatives from upper AlbianCenomanian sections in Brazil
and Ecuador. Included in the elaterate complex are Alaticolpites, Elaterocolpites, Elateroplicites, Elateropollenites,
Elaterosporites, Galeacornea, Pentapsis, Regalipollenites, Senegalosporites and Sofrepites. All possess elater-like protuberances, but are otherwise morphologically disparate. Ultrastructural analyses of three taxa, Elateroplicites africaensis,
Elaterosporites klaszii and Sofrepites legouxiae, reveals granular-alveolate ektexine and wall organization comparable to
that of gnetalean pollen and to fossil Equisetosporites=Ephedripites. A correlation exists between diversity=frequency
levels of Elaterates and successive events in opening of the northern part of the South Atlantic Ocean. This is interpreted
to reflect rapid diversification of the gnetalean sources of elaterate pollen in response to climatic perturbations associated
with opening and enlargement of this ocean. The introduction and diversification of Elaterates coincides with early
phases of angiosperm diversification, whereas extinction of the Elaterates-producing gnetalean group at the close of the
Cenomanian heralded the rise to dominance of angiosperms in low latitudinal areas fringing the northern South Atlantic.
1999 Elsevier Science B.V. All rights reserved.
Keywords: pollen; ultrastructure; gnetalean; mid-Cretaceous; Brazil; Ecuador

1. Introduction
The idea that part of northern South America
and northern Africa supported tropical vegetation in
Cretaceous times was first postulated in palynologi Corresponding

author. Fax: C55-21-2803318;

E-mail: [email protected]

cal literature during the late 1960s by Boltenhagen

(1967), Jardine (1967), and Brenner (1968). In the
1970s new data in support of this, including some
from several African countries, were provided by
Jardine et al. (1972, 1974a,b), Herngreen (1973a,b,
1974, 1975a,b), Brenner (1976), Vakhrameev (1978)
and Srivastava (1978, 1981, 1994). Subsequently, in
recognition of the importance of the palynological

0034-6667/99/$ see front matter 1999 Elsevier Science B.V. All rights reserved.
PII: S 0 0 3 4 - 6 6 6 7 ( 9 8 ) 0 0 0 7 6 - 1

202

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

data to our understanding of climatic mechanisms

that operated during opening of the South Atlantic
Ocean, Herngreen and Chlonova (1981) defined the
West AfricaSouth America (WASA) province for
pre-Albian Cretaceous times and the AfricaSouth
America (ASA) province for AlbianCenomanian
times. These provinces, now referred to as preAlbian, Early Cretaceous Dicheiropollis etruscus=
Afropollis province, and AlbianCenomanian Elaterates province, respectively (Herngreen et al., 1996),
occur within a few degrees latitude of the postulated
palaeoequator, and are recognized in several South
American countries (Brazil, Colombia, Ecuador,
Peru, Surinam, Venezuela), African countries (Algeria, Angola, Congo, Egypt, Gabon, Guinea-Bissau,
Ivory Coast, Libya, Mali, Morocco, Niger, Nigeria,
Senegal, Sudan, Zaire), the Middle East (Israel, Iraq,
Kuwait, Saudi Arabia), Bahama Islands, southern
Alps, westernmost China and Papua-New Guinea.
The AlbianCenomanian Elaterates province has
a unique palynoflora, characterized by the occurrence of many important pollen groups, the most
conspicuous being a group of pollen bearing morphological features known as elaters (Stover, 1963).
The complex comprises a diverse suite of morphologically bizarre forms that are characterized by
exinal outgrowths or projections that only superficially resemble elaters (s. str. as are associated with
spores of extant Equisetum). Several genera have
been defined to encompass these forms, including
Alaticolpites Regali, Uesugui et Santos, 1975, Elaterocolpites Jardine et Magloire, 1965, Elateroplicites
Herngreen, 1973, Elateropollenites Herngreen, 1973,
Elaterosporites Jardine, 1967, Galeacornea Stover,
1963, Pentapsis Lammons, 1970, Regalipollenites
Lima, 1980, Senegalosporites Jardine et Magloire,
1965, and Sofrepites Jardine, 1967. The projections
vary enormously in size, shape, and position, and
are either elater-like, horn-like, or resemble small
knobs. Other characters of the fossils are extremely
variable; they may be ellipsoidal, spherical, hemispherical, fusiform, or pentahedral in body shape;
and the sculpture ranges from smooth to conspicuously ornamented. Their apertural characters are not
well understood or well documented, although most
were thought to be inaperturate.
The affinity of the elaterate complex has intrigued
palynologists for several decades. There is some un-

certainty as to whether they represent spores of freesporing plants or pollen of seed plants (Stover, 1963;
Elsik, 1974; Srivastava, 1984). Indeed it is unknown
whether they were shed by members of a botanically united group or by plants of diverse botanical
origins, although Crane (1988, 1996) speculated that
they may represent specialized forms of gnetalean
pollen adapted to insect pollination. Species of the
elaterate complex occur in high abundances only in
the circum-Atlantic basins of northern South America and northern Africa, and only during the late
Albian to Cenomanian (cf. Fig. 1; Crane, 1996), suggesting that this area could have been the radiation
and diversification centre of the complex.
The purpose of this paper is to provide a review
of the species assigned to the respective genera of
elaterate pollen, examine their varied morphologies
through light microscope (LM), scanning electron
microscope (SEM), and transmission electron microscope (TEM) analyses, with aims of elucidating
whether or not their morphological and=or structural
attributes indicate a botanical affinity.

2. Material and methods

The specimens studied have been obtained from
strata of late Albian to Cenomanian age in Brazil and
Ecuador (Fig. 1). Samples containing abundant and
well preserved assemblages of Elaterates are from
Brazilian and Ecuadorian sections as detailed in
Fig. 2. The majority of the material comes from the
Caju Group in the Barreirinhas Basin, northeastern
Brazil (Fig. 2a). This is a sequence of interbedded
shale and shallow marine carbonates. Other specimens are from outcrop samples of the Itapecuru
Formation in the Parnaba Basin, northeastern Brazil.
Material from Ecuador is derived from the Napo Formation exposed in Rio Misahualli and Rio Chapiza,
in the northwest and southern parts of the Oriente
Basin, respectively (Fig. 2b). Previous observations
have been made on material from Brazil by Muller
(1966), Herngreen (1973a,b, 1974, 1975a,b), and
from Ecuador by Jaillard et al. (1994).
Samples were processed using standard palynological preparation methods (Dettmann, 1963;
Phipps and Playford, 1984; Wood et al., 1996).
The data on age and stratigraphic distribution of

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

203

44

42
20

WELL
IN-1

BARREIRINHAS BASIN

SO
BR
ADI
NHO
OUTCROP
AREA

PLATFORM

PARNABA BASIN
0

50

100 Km

ECUADOR

AN
CE
O
C
TI
AN
AT
L

81

79

77

CO
LO
EC MBI
A
UA
DO
R

50 100 Km

QUITO

COASTAL
PROVINCE

MOUNT
AINS

RIO
MISAHUALLI

ANDES

PACIFIC OCEAN

BRAZIL

ORIENTE BASIN

RIO
CHAPIZA

OR
AD
RU
PE

U
EC

Fig. 1. Locality map showing the basins in Brazil and Ecuador from where sample material was obtained.

204

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

(a)

(b)

Fig. 2. Montage showing the stratigraphic columns for the Cretaceous sections of (a) Brazil and (b) Ecuador.

elater-bearing grains were derived from routine lightmicroscopic analysis of several well cores and cuttings samples from wells drilled by Petrobras in all
coastal basins of northeastern Brazil, and outcrop
samples collected by Amoco from Ecuador.
For light microscope (LM) analyses, residues
were mounted in Entelan and covered with No. 0
coverslips. Photographs were taken under oil immersion using either an Axioplan Zeiss Microscope
(Brazilian forms) or a Zeiss Photomicroscope III

(Ecuadorian forms). For scanning electron microscope (SEM) analyses, grains were picked from
residues mixed in alcohol using a micromanipulator
and transferred to a specified section of a ruled aluminum square; after drying they were vacuum coated
with gold-palladium and examined with a Jeol JXA840A scanning electron microscope. Photographs of
whole grains and their specific morphological features were taken at 15 or 20 kV, respectively.
For transmission electron microscope (TEM)
analyses, specimens were picked from residues
mounted in alcohol using a micromanipulator and
transferred to a thermonox coverslip smeared with
adhesive. A drop of 1% agar was added and the
specimens stained in osmium tetroxide for 2 hours,
followed by uranyl acetate for 1 hour, and then
surface embedded in Spurrs medium following the
method of Milne and McCaul (see Milne, 1994,
1998). Sections were cut with a diamond knife,
stained with lead citrate, and examined using a Jeol
1010 instrument.
Frequency and diversity levels of Elaterates are
based on a synthesis of palynofloral assemblages
represented in late AptianCenomanian sequences
of equatorial and marginal basins of Brazil. Quantitative analyses were carried out on a range of
palyno-assemblages from each of the successive palynostratigraphic zones delineated for the Albian
Cenomanian of Brazil (Table 2; Fig. 3). Relative
abundance levels of Elaterates are with reference to
the other major groups (spores, polyplicates, Classopollis, angiosperm pollen, and others) represented
in the palynofloras. Diversity levels of Elaterates and
the stratigraphic ranges of the individual species represented are detailed for the late AptianTuronian of
Brazil (Fig. 4).

3. Systematics
Table 1 summarizes the pollen morphological data
and bibliographic references for the pollen discussed
in this paper. This includes the characteristics of
the body, ornament, and appendages of the elaterate complex. Data for Galeacornea clavis Stover
are derived from Stovers (1963) original descriptions because we did not observe this species in
our studies. For the sake of completeness we con-

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

205

Fig. 3. Relative frequency levels of Elaterates and other sporepollen groups in assemblages from the upper AptianCenomanian of
Brazil.

sider it important to summarize those data here. A

brief discussion of Alaticolpites Regali, Uesugui et
Santos, Elateropollenites Herngreen, Pentapsis Lammons, Regalipollenites Lima, and Senegalosporites
Jardine et Magloire, is given at the end of this
section because these taxa possess elater-like projections, which, however, are unlike those found in
other genera.
Genus Elaterocolpites Jardine et Magloire, 1965
1965 Elaterocolpites Jardine et Magloire, p. 206.
1967 Elaterocolpites Jardine et Magloire emend.
Jardine, p. 247.
1984 Elaterocolpites Jardine et Magloire emend.
Srivastava, p. 232.
Type: Elaterocolpites castelainii Jardine et Magloire,
1965. Monospecific genus consisting of Elaterocolpites castelainii.
Elaterocolpites castelainii Jardine et Magloire, 1965
(Plate I, 15)

1965 Elaterocolpites castelainii Jardine and Magloire, p. 206, pl. 4, figs. 6, 7.

Dimensions: (30 specimens) body 3553 m (long
axis), appendages 610 m wide and 1830 m
long.
Comments: Jardine (1967) re-examined the type material of Elaterocolpites castelainii, and subdivided
this species into two subforms. Form A has a
narrow annular ring surrounding the corpus, which
he attributed to a young or immature grains. Form
B corresponds to the mature grains and has well
stretched appendages. In the Brazilian material another subform named here Form C (Plate I, 3) is
distinct from the others in being bigger and having
two solid globular expansions at the ends of the long
axis of the corpus. Herngreen (1974, pl. III, fig. 5)
illustrated a specimen similar to Form C, which he
called Form A of Jardine (1967). All these forms
occur frequently in upper Albianmiddle Cenomanian strata of the Caju Group in the Barreirinhas
basin.

206

Table 1
Pollen morphological data and bibliographic references to species of the elaterate complex
Species

Body

Ornamentation
size

wall

Alaticolpites limai

ellipsoidal to subspherical

L: 7072 m
S: 4868 m

13 m

Elaterocolpites
castelainii

ellipsoidal to subspherical

Elateroplicites
africaensis

Bibliographic reference

shape

number size

smooth

flap-shaped

10

W: 1222 m
L: 2040 m

Regali et al. (1975a,b)

4050 m

smooth to
microgranular

cylindrical

10

W: 610 m
L: 1830 m

Jardine and Magloire

(1965)

ellipsoidal

L: 3562 m
S: 2541 m

smooth

long, slender

2 or 4

W: 36 m
L: 2080 m

Herngreen (1973a,b)

Elateropollenites
jardinei

subtriangular

3045 m

11.5 m

thinly striate

short, slender

2 or 3

W: 35 m
L: 311 m

Herngreen (1973a,b)

Elaterosporites
acuminatus

sub-hemispherical

L: 3852 m
S: 2035 m

<1 m

spinose

U-shaped

W: 610 m
L: 3036 m

Stover (1963), Jardine

(1967)

Elaterosporites
klaszii

ellipsoidal

L: 3552 m
S: 2535 m

smooth

U-shaped

W: 46 m
L: 4560 m

Jardine and Magloire

(1965), Jardine (1967)

Elaterosporites
protensus

ellipsoidal

L: 5073 m
S: 3042 m

verrucate=
spinose

U-shaped

W: 46 m
L: 3040 m

Stover (1963), Jardine

(1967)

Elaterosporites
verrucatus

ellipsoidal

L: 5575 m
S: 3543 m

verrucate

U-shaped

W: 46 m
L: 3040 m

Jardine and Magloire

(1965), Jardine (1967)

Galeacornea causea

ellipsoidal

L: 3057 m
S: 2342 m

13 m

smooth

zona, rather than

appendages

W: 2738 m
L: 1015 m

Stover (1963)

Galeacornea clavis a

ellipsoidal

L: 4050 m
S: 2535 m

11.5 m

smooth

Y-shaped horn and

equatorial zona

W: 35 m
L: 3050 m

Stover (1963)

Pentapsis valdiviae

pentagonal

L: 5075 m
S: 4555 m

thinly punctate

flap-shaped

W: 913 m
L: 3055 m

Lammons (1970)

Regalipollenites
amphoriformis

ellipsoidal

L: 3070 m
S: 2530 m

plicate

cylindrical

W: 36 m
L: 615 m

Lima (1980)

Senegalosporites
costatus

cylindrical to fusiform

L: 4575 m
S: 2040 m

twisted plicate

cylindrical

W: 36 m
L: 715 m

Jardine and Magloire

(1965)

Senegalosporites
petrobrasi

cylindrical to fusiform

L: 60100 m
S: 2535 m

straight plicate

cylindrical

W: 46 m
L: 1020 m

Herngreen (1974)

Sofrepites legouxiae

subspheroidal, ellipsoidal
or subtetrahedral

L: 2044 m
S: 2138 m

smooth to
infragranulate

short, stubby

2 or 3

W: 46 m
L: 1221 m

Jardine (1967)

a Derived

from Stover (1963).

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

body shape

Appendages

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

207

Fig. 4. Stratigraphic range and diversity levels of Elaterates during the mid-Cretaceous in Brazil.

Genus Elateroplicites Herngreen, 1973

1973b Elateroplicites Herngreen, p. 550.
Type: Elateroplicites africaensis Herngreen, 1973,
by original designation. Monospecific genus consisting of Elateroplicites africaensis.
Elateroplicites africaensis Herngreen, 1973 (Plate II,
15; Plate III, 16; Plate IV, 16)
1967

Incertae sedis forma A, Jardine, p. 255, pl.

III, figs. KM.
1973b Elateroplicites africaensis Herngreen, p. 550,
pl. 5, figs. 57.
Description: Ellipsoidal grains comprising a smooth
exinal body formed by 34 exterior ribs. These ribs
or bands are separated by narrow furrows averaging 1 m in width, and exhibit a strong tendency
towards twisting along the long axis of the grain;
occasional specimens are not twisted (Plate III, 6).
Usually two of the ribs project beyond the body

and form 2, or rarely, 4 long, slender appendages.

The appendages are smooth, solid, flexible, of equal
length, but slightly thicker at the termination and are
always turned towards one surface of the grain, suggesting that the opposite surface may represent the
internal face (proximal) with respect to the tetrad.
The ribs surrounding the longitudinal axis converge
and fuse(?) at the end of the axis. SEM photomicrographs (Plate IV, 5, 6) illustrate the twisting and
tapering of the ribs towards one centre of convergence where they fuse in a manner similar to the
ribs of polyplicate forms included within Equisetosporites and Ephedripites. No germinal aperture or
columellate layer of the exine are discernible under
LM. The dimensions of this species (based on 30
specimens) are body 3562 m (long axis), 2541
m (short axis), ribs 325 m wide, 23 m thick,
appendages 36 m wide and 2080 m long.
Ultrastructure: Pollen wall composed of ektexine
which is differentiated into three zones (Plate IV,
2, 3). Innermost zone 0.5 m thick, homogeneous,

208

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

continuous and of uniform thickness in all regions

of palynomorph; middle zone thin (<0.2 m thick),
discontinuous being confined to ribs and appendages,
granulate in structure, the granules separated by alveolae which are larger in central portions of the infratectum. Outer ektexine of variable thickness (up to
2 m thick), homogeneous in structure, forms outer
surface of ribs and appendages. Finely granular material discontinuously overlies the tectum, and may
be unrelated debris.
Discussion: The disposition of the ribs and the extension of two of these is confirmed from SEM analyses

(Plate III, 4, 5). Ultrathin sections suggest that the

wall is analogous to ektexine with homogeneous
tectum, granulate to alveolate infratectum and homogeneous foot layer. The tectum, infratectum and foot
layer form the ribs which are separated by narrow
grooves floored by a thin foot layer. Apertures appear to be lacking, but sections transverse to the long
axis confirm two expanses (up to 12 m) of the foot
layer folded beneath the ribs on opposite sides of the
pollen, and it is possible these may have served as
germinal apparatuses.

PLATE I
Elaterocolpites castelainii Jardine et Magloire, 1965. Specimens from Brazil (25) and Ecuador (1). 750 unless specified otherwise.
1.
Elaterocolpites castelainii Form B. 840.
2.
Elaterocolpites castelainii Form A, showing a sharply defined corpus.
3.
Elaterocolpites castelainii Form C, specimen with a globular expansion of the exine at each end of the long axis of the grain.
4, 5.
Elaterocolpites castelainii Form B, SEM of whole grains with large appendages. 1400.
PLATE II (see p. 210)
Elateroplicites africaensis Herngreen, 1973. Specimens from Brazil (13) and Ecuador (4, 5). 750 unless specified otherwise.
1, 2.
View showing arrangement of ribs at ends of long axis of pollen.
35.
Showing twisted ribs. 840.
PLATE III (see p. 211)
Elateroplicites africaensis Herngreen, 1973. Specimens from Brazil. 750 unless specified otherwise.
1, 2.
Specimens with four appendages.
3.
Specimen with two appendages and twisted ribs.
4, 5.
SEM of specimen showing ribs that taper towards the end of the long axis.
4.
1000.
5.
1400.
6.
SEM showing parallel ribs that taper and converge at the end of the long axis. 1000.
PLATE IV (see p. 212)
Elateroplicites africaensis Herngreen, 1973. Specimens from Brazil.
1.
TEM image. Section cut perpendicular to equatorial plane showing thin foot layer (arrows) folded beneath thicker exine of the
ribs. 2000.
2, 3.
TEM images. Section showing homogeneous tectum (T), granulate-alveolate infratectum (G) and thinner foot layer (F). Note
the tectum and infratectum are discontinuous and thin abruptly towards the grooves separating the ribs.
2.
6000.
3.
12,000.
4.
TEM image. Section through a rib showing alveolate infratectum. 12,000.
5, 6.
SEM images. 800.
PLATE V (see p. 213)
Specimens from Brazil (13, 6) and Ecuador (4).
1, 3.
Elaterosporites acuminatus (Stover) Jardine, 1967, showing slender horns characteristic of the species. 750.
2, 46. Elaterosporites verrucatus (Jardine et Magloire) Jardine, 1967. Examples illustrating sculptural range of the species.
2, 5, 6. 1000.
4.
840.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE I

209

210

PLATE II

For description see p. 208.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE III

For description see p. 208.

211

212

PLATE IV

For description see p. 208.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE V

For description see p. 208.

213

214

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

Genus Elaterosporites Jardine, 1967

1967 Elaterosporites Jardine, p. 240.
Type: Elaterosporites verrucatus (Jardine et Magloire) Jardine, 1967.
Elaterosporites acuminatus (Stover) Jardine, 1967
(Plate V, 1, 3)
1963 Galeacornea acuminata Stover, p. 89, pl. 2,
figs. 810, text-fig. 6.
1967 Elaterosporites acuminatus (Stover) Jardine,
p. 246, pl. 3, figs. D, E.

Dimensions: (5 specimens): body 4265 m (long

axis) and 2540 m (short axis); appendages 46
m wide and 2842 m long.
Discussion: This species is relatively rare in our
material. As already pointed out by Stover (1963),
Elaterosporites acuminatus is very similar to E. protensus. The distinction is based mainly in the shape
and size of the body, that is slightly smaller and less
convex in E. acuminatus; on the ends of the horns,
that are slender in E. acuminatus, and rounded in
E. protensus; and on the width of the annular ring
at the flat face which is narrower in E. acuminatus.

PLATE VI
Specimens from Brazil (13, 5) and Ecuador (4, 6).
1, 3. SEM of Elaterosporites verrucatus (Jardine et Magloire) Jardine, 1967. 1400.
2.
Elaterosporites verrucatus (Jardine et Magloire) Jardine, 1967. 750.
46. Elaterosporites klaszii (Jardine et Magloire) Jardine, 1967.
4, 6. 840.
5.
750.
PLATE VII (see p. 216)
Elaterosporites klaszii (Jardine et Magloire) Jardine, 1967. Specimens from Brazil.
1.
SEM image showing planar face with very thin exine surrounded by annular ring. 1700.
2.
LM view focused on planar face and annular ring. 750.
3, 4. SEM images showing convex face. 1200.
5, 6. Lateral and oblique views. 750.
PLATE VIII (see p. 217)
Elaterosporites klaszii (Jardine et Magloire) Jardine, 1967. Specimens from Brazil.
1, 2. TEM images. Sections cut parallel to equatorial plane.
1.
1500.
2.
3000.
3, 4. TEM images. Detail of exine showing thin tectum (T), granulate to alveolate infratectum (G), and thin foot layer (F) underlain by
endexine (En).
3.
10,000.
4.
12,000.
5.
SEM image showing planar and convex faces. 1200.
6.
LM image. 750.
PLATE IX (see p. 218)
Specimens from Brazil (26) and Ecuador (1). 750 unless specified otherwise.
15. Elaterosporites aff. E. klaszii Jardine, 1967, showing narrow annular ring characteristic of this form.
1.
840.
6.
Elaterosporites protensus (Stover) Jardine, 1967, showing conspicuous sculpture on convex face.
PLATE X (see p. 219)
Elaterosporites protensus (Stover) Jardine, 1967. Specimens from Brazil (1, 36) and Ecuador (2). 750 unless specified otherwise.
15. LM images of specimens in different orientations.
2.
840.
4.
Note the appendages form a broad circular ring. 1000.
6.
SEM of convex face. 1000.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE VI

215

216

PLATE VII

For description see p. 214.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE VIII

For description see p. 214.

217

218

PLATE IX

For description see p. 214.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE X

For description see p. 214.

219

220

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

In our material only the sharp tipped horns in E.

acuminatus can be used to distinguish between the
two species.
Elaterosporites verrucatus (Jardine et Magloire)
Jardine, 1967 (Plate V, 2, 46; Plate VI, 13)
1965 Galeacornea verrucata Jardine et Magloire, p.
204, pl. 3, figs. 2831.
1967 Elaterosporites verrucatus (Jardine et Magloire) Jardine, p. 244, pl. 2, figs. EG, pl.
3, fig. G.
Dimensions: (35 specimens): body 5575 m (long
axis) and 3543 m (short axis); appendages 46
m wide and 3040 m long.
Elaterosporites klaszii (Jardine et Magloire) Jardine,
1967 (Plate VI, 46; Plate VII, 16; Plate VIII, 16)
1963 Galeacornea sp., Stover, p. 89, pl. 2, figs. 16,
17.
1965 Galeacornea klaszi Jardine and Magloire, p.
205, pl. 4, figs. 2, 3.
1967 Elaterosporites klaszi (Jardine and Magloire)
Jardine, p. 246, pl. 3, figs. HN.
Dimensions: (35 specimens): body 3552 m (long
axis), 2535 m (short axis); appendages 46 m
wide and 4560 m long.
Ultrastructure: Exine comprises a thin endexine of
uniform electron density and near homogeneous in
structure overlain by thicker ektexine composed of
a thin homogeneous inner layer (foot layer) beneath
an irregularly granulate to alveolate infratectum and
a homogeneous tectum. Infratectum and tectum of
variable thickness; thickest on horn bearing surface and beneath cingulum, and thinnest on planar
surface, the central regions of which appear to be
composed solely of foot layer. Infratectum more
loosely structured (i.e., alveolae larger) towards tectum interface than at foot layer interface.
Comments: After re-examination of the original material, Jardine (1967) created the species
Elaterosporites sp. aff. E. klaszii (Plate IX, 15) to
accommodate forms, essentially similar to E. klaszii,
but having a narrower annular ring. We consider
that is not as distinctive at the specific level. This
species is known as recycled in Cretaceous deposits
of Alabama (Gregory and Hart, 1992).

Elaterosporites protensus (Stover) Jardine, 1967

(Plate IX, 6; Plate X, 16)
1963 Galeacornea protensa Stover, p. 88, pl. 2, figs.
1115, text-fig. 5.
1967 Elaterosporites protensus (Stover) Jardine, p.
244245, pl. 3, figs. AC.
Dimensions: (30 specimens): body 5073 m (long
axis) and 3042 m (short axis); appendages 46
m wide and 3542 m long.
Discussion: Stover (1963, pl. 2, fig. 15) figures an
unexpanded specimen that he argued suggested
formation of the pollen in tetrads with the flat surface orientated towards the centre of the tetrad (i.e.,
proximal). An alternative interpretation is that in
the young tetrad phase the unexpanded pollen are
aligned with their sculptured, horn-bearing surface
directed towards the centre of the tetrad. In the mature tetrad phase expansion may have been confined
to the horn-bearing surface and was perhaps associated with separation of the individuals of the tetrad.
Thus, it is feasible that the convex surface may be
proximal to the original tetrad.
Genus Galeacornea (Stover) Jardine, 1967
1963 Galeacornea Stover, p. 86.
1967 Galeacornea Stover emend. Jardine, pp. 237
240.
Type: Galeacornea clavis Stover, 1963.
Comments: The genus Galeacornea was described
by Stover (1963) and included four elater-bearing
pollen. Two of these species, G. causea and G. clavis
remain in the genus, the other two, G. acuminatus and G. protensus, were transferred to the genus
Elaterosporites by Jardine (1967). Subsequent studies by Zhang and Zhan (1986) resulted in the description of Galeacornea tarimensis, a species so far not

PLATE XI
Galeacornea causea Stover, 1963. Specimens from Brazil (14,
6) and Ecuador (5).
1, 3.
Form A of Jardine (1967), possibly representing immature grains. 1400.
2, 46. Form B of Jardine (1967), the most common form of
the species, in a range of orientations.
2, 4, 6. 1400.
5.
840.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE XI

221

222

PLATE XII

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

recorded from Ecuador or Brazil. G. clavis, which

has hitherto been known only from West Africa, has
recently been found (E.H. Roesner, Petrobras, pers.
commun.) in the Ceara Basin, northeastern Brazil.
Galeacornea causea Stover, 1963 (Plate XI, 16;
Plate XII, 13)
1963 Galeacornea causea Stover, p. 87, pl. 1, figs.
16, 17; pl. 2, figs. 17, text-fig. 4.
Dimensions: (20 specimens): body 3057 m (long
axis) and 2342 m (short axis); flaps 2738 m
wide and 1015 m high.
Comments: Jardine and Magloire (1965) did not consider Galeacornea causea and G. clavis as two useful
species because of the general similarities of their
morphology, co-occurrence, identical stratigraphic
range, and the scarcity of Galeacornea causea like
specimens. They concluded that G. causea was a variant of G. clavis. Later, Jardine (1967) re-examined the
original material and agreed with the maintenance of
the two species, and distinguished two varieties of G.
causea, naming them Form A and Form B. According to Jardine (1967), Form A includes immature
specimens and Form B, which has a lobed appearance, contains mature ones. In our Brazilian samples
Form A is very rare and Form B is Abundant.
Genus Sofrepites Jardine, 1967
1967 Sofrepites Jardine, p. 248.
1981 Sofrepites Jardine emend. Jingxian, p. 98.
1982 Sofrepites Jardine emend. Boltenhagen, p. 150.
Type: Sofrepites legouxiae Jardine emend. Jingxian,
1981.
Comments: Jingxian (1981) emended the description
of Sofrepites based on the unequal length of the
projections. The quality of the illustrations make it

PLATE XII
Specimens from Brazil.
12. Galeacornea causea Stover, 1963, SEM images of planar
face of grain.
1.
1700.
2.
2000.
3.
Galeacornea causea Stover, 1963, LM view. 1400.
46. Sofrepites legouxiae Jardine, 1967, LM views. 1400.

223

difficult to ratify this emended description. The illustrations seem to be of a polyplicate pollen grain similar to pollen belonging to the genus Regalipollenites
Lima, 1980 and thus there is doubt as to whether
the Jingxian (1981) specimens belong in Sofrepites.
Boltenhagen (1982) also emended the generic description but this was not accepted by Jansonius and
Hills (19761996, card 4164) as the type of the
genus was excluded. Jansonius and Hills proposed
the new name Sofrepites boltenhagenii for the taxon
described by Boltenhagen (1982) in accordance with
the ICBN (1994).
Horowitz (1970) described Sofrepites michali
from southern Israel, however, the illustration (pl.
III, fig. 8) appears to show a fragment of a species
of Elaterosporites. The fragmentary nature of the
specimen and doubts surrounding its inferred age
(Late Jurassic) renders this record highly suspect
(see Herngreen, 1974, p. 520). As such this species
is considered invalid as it is based on a fragment.
Sofrepites legouxiae Jardine, 1967 (Plate XII, 46;
Plate XIII, 16; Plate XIV, 15)
1967 Sofrepites legouxae, Jardine, p. 255, pl. 3, Figs.
H, J; text-fig. 5.
Description: Subspherical to ellipsoidal body with a
subcircular, elliptical or convexly subtriangular outline where 2 or 3 smooth, solid appendages of equal
length project. Monocolpate; colpus parallel to long
axis of grain, extends almost to the border where
its extremities are spatulate. In some specimens the
aperture is clearly visible but in others is covered
by a very thin exinal layer. Exine smooth to infragranulate, approximately 1 m thick. Dimensions
(50 specimens): body 2045 m (long axis), 2042
m (short axis); colpus 2242 m long and 25 m
wide; appendages 36 m wide and 721 m long.
Ultrastructure: Exine with ektexine comprising outer
homogeneous zone (tectum) of uniform electron
density and of variable width, a middle zone (infratectum) that is granulatealveolate in structure
and up to 3 m in thickness, and a thin inner zone
(foot layer). A very thin layer (endexine) with faintly
lamellate structure is discernible (Plate XIII, 3, 4) in
some sections. The tectum and infratectum are thickest in the interapertural areas of the grain and on the
appendages, and are very thin or absent at the mar-

224

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

gins of the colpus; infratectum with larger alveolae

at tectum interface adjacent to the foot layer.
Discussion: Scanning electron microscopic analyses
confirm the pollen is monocolpate (Plate XIII, 6;
Plate XIV, 5) and that the exine is tectate granulate.
Genus Elateropollenites Herngreen, 1973 (Plate
XIV, 6; Plate XV, 14)
1965

Incertae sedis CI. 50 Jardine et Magloire, p.

207.
1973b Elateropollenites Herngreen, p. 549.

Type: Elateropollenites jardinei Herngreen, 1973.

Comments: Herngreen (1973b) created this genus
to accommodate pollen with elater-like appendages.
The type species Elateropollenites jardinei possesses
a swollen body and 3 appendages thickened at their
extremities (Herngreen, 1973b, p. 531, pl. IV, figs. 5
8). Herngreen differentiated Elateropollenites from

Elaterocolpites, Elaterosporites, and Sofrepites, on

the basis of number of appendages, the shape of
appendages, and the size of the body, but suggested
that the appendages in E. jardinei were similar to
those of Elaterocolpites castelainii. We have not
studied this species even though it is recorded in
lower Albian sediments in Brazil.
Regali (1989), and Regali (in Regali and Viana,
1989) described three species, E. bicornis, E. dissimilis, and E. praecursor, and differentiated them
on the basis of elater length. Further, Regali (1989)
emended the genus Elateropollenites Herngreen to
include forms with large variations in size of the
elaters, but such variation was accounted for in the
original generic description.
Genus Regalipollenites Lima, 1980 (Plate XV, 5, 6)
1975 Steevesipollenites amphoriformis Regali, Uesugui et Santos, p. 271.

PLATE XIII
Sofrepites legouxiae Jardine, 1967. Specimens from Brazil.
1, 2. TEM images. Sections cut perpendicular to equatorial plane through appendages.
1.
2500.
2.
1500.
3, 4. TEM images. Detail of exine showing homogeneous tectum (T), granular layer (G), thin foot layer (F) and endexine (En).
3.
6000.
4.
8000.
5, 6. SEM images.
5.
1100.
6.
Note monocolpate aperture. 1900.
PLATE XIV (see p. 226)
Specimens from Brazil (1, 2, 46) and Ecuador (3).
1, 3. Dyads of Sofrepites legouxiae Jardine, 1967.
1.
1400.
3.
840.
2.
Sofrepites legouxiae Jardine, 1967, showing the monocolpate aperture and (in this case) only two short appendages. 1400.
4, 5. SEM images of Sofrepites legouxiae Jardine, 1967 showing the monocolpate aperture. 2000.
6.
Elateropollenites jardinei Herngreen, 1973, focused on striations of the corpus. 1400.
PLATE XV (see p. 227)
Specimens from Brazil.
1, 3. SEM images of Elateropollenites jardinei Herngreen 1973.
1.
Showing three appendages. 2200.
3.
2600.
2, 4. Elateropollenites jardinei Herngreen, 1973 showing central sulcus (doubtful aperture) and striations. 1400.
56. Regalipollenites amphoriformis (Regali et al.) Lima, 1980.
5.
With a ?monocolpate aperture. 750.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE XIII

225

226

PLATE XIV

For description see p. 224.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

PLATE XV

For description see p. 224.

227

228

PLATE XVI

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

1980 Regalipollenites Lima, p. 45.

Type: Regalipollenites amphoriformis (Regali et al.)
Lima, 1980. Monospecific genus consisting of Regalipollenites amphoriformis.
Comments: Lima (1980) created this genus to accommodate polyplicate pollen grains of unequal exine thickness=extension at opposing ends of the long
axis of the grain. The type species Regalipollenites
amphoriformis is polyplicate with a long appendage
at one end and a small knob on the other end of
the ellipsoidal to fusiform grain. Lima (1980) placed
Regalipollenites in the polyplicate group including
Steevesipollenites amphoriformis (described by Regali et al., 1975a); but is similar also to the elaterates
in possession of long elater-like appendages. Furthermore, R. amphoriformis, shows some similarity
to Elateroplicites africaensis and to Ephedriptes=Equisetosporites in its possession of longitudinal ribs.
Genus Pentapsis Lammons, 1970 (Plate XVI, 2, 4)
1970 Pentapsis Lammons, p. 175.
Type: Pentapsis valdiviae Lammons, 1970. Monospecific genus consisting of Pentapsis valdiviae.
Comments: Of all the genera discussed in this paper
Pentapsis is the most disparate morphologically and
may be unrelated to the other elater-bearing genera.
Lammons (1970) erected Pentapsis to accommodate
pollen grains that contain buttress-like structures that
are terminally attached at more-or-less equal angles
around the periphery of each of two parallel pentagonal polar plates, and therefore connecting the two
plates. The buttress morphology gives an appearance
of elater-like projections, with slight resemblance
to Sofrepites legouxiae or Elaterocolpites castelainii.

229

This species is restricted in Brazil to sediments of

early Albian age.
Genus Senegalosporites Jardine et Magloire, 1965
(Plate XVI, 1, 3)
1965 Senegalosporites Jardine et Magloire, p. 208.
1974 Senegalosporites Jardine et Magloire emend.
Herngreen, p. 548.
Type: Senegalosporites costatus Jardine et Magloire,
1965, by original designation.
Comments: The genus Senegalosporites Jardine et
Magloire, 1965, is represented by a cylindrical to
fusiform grain with twisted or straight ridges resembling the general organization of the polyplicate
pollen group. The ridges, along the long axis of the
grain, usually fuse at the ends and form a conspicuous protrusion similar to an elater-like appendage.
The type species is characterized by twisted ridges.
Herngreen (1974) broadened the generic diagnoses
of Senegalosporites to include pollen grains with
straight ridges and erected the species S. petrobrasi.
Regali et al. (1975b, p. 271, pl. VI, fig. 1), misinterpreted the morphology of the polar appendages
and placed S. petrobrasi into Steevesipollenites, and
created S. duplibaculum. Re-examination of the original material of Steevesisporites duplibaculum reveals a striking similarity to S. petrobrasi Herngreen. Additionally, the elater-like appendages bear
a slight resemblance to those of Sofrepites legouxiae.
Jingxians (1981) species, Senegalosporites minor
and S. mirifus, are here interpreted as polyplicate
grains conformable with Steevesipollenites. Senegalosporites is rare in Brazil and is restricted to late
Albian to Cenomanian aged deposits.
Genus Alaticolpites Regali, Uesugui et Santos, 1975
(Plate XVI, 5, 6)

PLATE XVI
Specimens from Brazil.
1. Senegalosporites costatus Jardine et Magloire, 1965. 1400.
2. Pentapsis valdiviae Lammons, 1970. Equatorial view.
1400.
3. Senegalosporites petrobrasi Herngreen, 1974. Note the parallel ridges. 1400.
4. Pentapsis valdiviae Lammons, 1970. Polar view. 1400.
5. Alaticolpites limai Regali, Uesugui et Santos, 1975. 1400.
6. SEM image of Alaticolpites limai Regali, Uesugui et Santos,
1975. 1400.

1975 Alaticolpites Regali, Uesugui et Santos, p. 288.

Type: Alaticolpites limai Regali, Uesugui et Santos,
1975. Monospecific genus consisting of Alaticolpites
limai.
Comments: Alaticolpites accommodates colpate
pollen of ellipsoidal to subspherical shape and
with 10 handle-shaped or leaf-like appendages. The
pollen is similar in some respects (general outline

230

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

and form of the flaps) to species of Galeacornea, differing in the form and number of appendages. Specimens attributed to Galeacornea causea by Brenner
(1968, pp. 353354, pl. III, figs. 45), and Schrank
and Ibrahim (1995, p. 12, pl. 2, figs. 910) from
the AlbianCenomanian of Peru and Egypt are conformable with Alaticolpites. In Brazil the genus is
restricted to strata of Albian age.

4. Botanical affinities
Affinities of elaterate pollen have remained obscure as they bear little morphological resemblance
to spores and pollen of extant taxa, and thus far
are unknown in situ from fossil plants. Stover
(1963) suggested that the presence of a sulcus- or
colpus-like germinal apparatus in some taxa implied an angiospermous or gymnospermous affinity.
Moreover, the nature of unexpanded examples of
Elaterosporites protensus, implied to Stover (1963)
that the individuals of the species probably formed in
a tetrad configuration. However, he found it difficult
to reconcile that the horn-bearing surface represented
the proximal face, and concluded that the taxon accommodates spores with the horns borne on the
distal surface. The possibility that some elaterate
pollen were borne in dyads is hinted at by specimens
attributed by Srivastava (1984) to Elaterocolpites
pentarhethus. Srivastavas figured specimens may
represent obligate dyads of Sofrepites, and moreover,
with sporopolleninous (?tapetal) material uniting the
proximal faces of the individuals. The colpi described by Srivastava may represent uneven breaks
between the individuals of the dyad, rather than
signifying an angiospermous origin of the grains.
Morphological relationships between elaters, auriculae, sacci, and thickenings found on gnetalean
and some angiospermous pollen were considered at
length by Elsik (1974) who concluded that a range
of morphologically disparate palynomorph taxa
(Galeacornea, Elateroplicites, Auriculiidites, Pediculisporis and others) represented ephedroid grains,
some perhaps shed from an intermediate gnetaleanmonocotyledonoid offshoot (?early Araceae) which
is now extinct or may in fact be representative of
early angiosperms (Elsik, 1974, p. 529). Trevisan
(1980) explored possible relationships between fos-

sil Ephedripites sp. from the Cretaceous of Italy and

pollen of extant Gnetales (Ephedra, Welwitschia) and
the monocotyledon Spathiphyllum (Araceae). From
comparative morphological and ultrastructural studies, she demonstrated that Ephedripites grains were
more similar to those of Ephedra and Welwitschia
than to those of Spathiphyllum. The exine of pollen
of the last mentioned genus possesses an infratectal
layer that is columellate in organization by contrast to the loosely granular infratectum of pollen of
extant gnetaleans (Kurman and Zavada, 1994; Rowley, 1996) and the compact granular infratectum of
the Italian Ephedripites. It should be noted, however, that collumellae-like rods have been reported
in fresh fixed grains of Ephedra foliata Bois et K.
ex C.A. Mey, but dried grains of the same species
have a granular infratectum (El-Ghazaly and Rowley,
1997).
Cretaceous ephedroid pollen assigned to Equisetosporites from Brazil are similar in exine ultrastructure and stratification to the elaterate pollen studied
by us and Ephedripites studied by Trevisan (1980)
and others (Lima, 1978, 1980; Osborn et al., 1993,
p. 171). The latter authors demonstrated a lamellated endexine overlain by ektexine characterized by
a granulate infratectum that is capped by a homogeneous tectum. Ektexine of the furrows separating
the ridges thins to a single homogeneous layer
(D tectum) that forms a folded, hinge-like structure
directly over the furrow; these furrows were interpreted to serve as potential apertures (Osborn et
al., 1993, p. 179, pl. 2, figs. 46). Regions of thin
exine that occur in the three elater taxa sectioned
by us (Plate IV, 2, 3; Plate VIII, 3, 4; Plate XIII,
3, 4) are probably analogous, but we interpret that
exine thinning involves the infratectum and tectum,
whereas the foot layer persists and thins little, if
any. A comparable persistence of the foot layer and
marked thinning of the tectum and infratectum has
been demonstrated for the furrow regions in pollen
of Ephedra (Van Campo and Lugardon, 1973, pl. 1,
fig. 4; Kurman and Zavada, 1994, fig. 32; Rowley,
1996, pl. 8, fig. 2).
Taking into account wall stratification and ultrastructural compatibility of Sofrepites, Elateroplicites
and Elaterosporites with that of Ephedripites and
other Cretaceous polyplicate pollen it is suggested
that elaterates and polyplicate pollen are botanically

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

related. Furthermore, based on ektexinous ultrastructural similarity to pollen of Ephedra and Welwitschia
relationships are suggested to be gnetalean and support earlier speculations by Crane (1988, 1996), who
suggested that Elaterates may represent a specialized
group of ephedroids adapted to insect pollination.
Although initially thought to be gnetalean, Triassic pollen assigned to Equisetosporites chinleana
Daugherty and Cornetipollis reticulata Pocock et
Vasanthy, both have an infratectum that is distinctly
columellate, and the Triassic pollen are thought to
be angiospermous (Zavada, 1984, 1990; Pocock and
Vasanthy, 1988).

231

and associated with diverse cryptogam spores comprising lycophytes, ferns and bryophytes. Palaeoenvironments are interpreted to have alternated between humid and drier phases. Marine incursions
occurred during the latest Aptian and a thick sequence of evaporites accumulated in what is interpreted to have been a hypersaline lacustrine setting.
Palynofloras in these sediments are characterized
by abundant Classopollis and an increase in polyplicate pollen whereas bisaccate pollen and cryptogam spores occur in low abundances. Angiosperm
pollen are present but restricted to monosulcate
(Clavatipollenites, Dichastopollenites, Stellatopollis,
Transitoripollis), zonosulcate (Afropollis), and small
tricolpate forms (most presumed to be of hamamelidid affinity).
A transgressive event in the latest Aptian heralded
the onset of marine conditions with deposition of
siliclastics interbedded with shallow platform carbonates and marls in the early Albian. Palynofloras
from these sediments are the oldest known elaterate
pollen (Elateropollenites jardinei) together with increased frequencies of angiosperms and increasingly
diverse dinocysts (Table 2; Fig. 3).
Diversity and frequency levels of the elaterates
climaxed during late AlbianCenomanian times (Table 2; Figs. 3 and 4). Other features of the Brazilian and Ecuadorian late AlbianCenomanian palynofloras are high frequencies of Classopollis, scarce
bisaccate pollen, and low diversity cryptogam assemblages. As such the palynofloras conform with those
that characterize the ASA phytogeographic province
of Herngreen and Chlonova (1981). The vegetation
of this low latitude region (Fig. 5) is considered to
have comprised dry-zone and=or mangrove communities of Cheirolepidaceae, perhaps with savannah
of gnetalean associations; climates are considered to
have been warm although the equator to pole temper-

5. Palaeoecological and palaeoclimatic

interpretations
An appreciation of elaterate-producing plants may
be gained from knowledge of associated vegetation
and the types of environments they inhabited. Associated plant fossils provide a perspective of the
vegetation and the enclosing sediments reflect the
interaction of physiographic=biotic processes in the
region.
The Cretaceous was a period of continental
breakup and drift and the initiation of new oceans
worldwide. In the northern Gondwana region the
South Atlantic Ocean was initiated with the separation of South America from Africa. Sequences
developed in the marginal basins of Brazil and western areas of northern Africa reflect the environments
during the initial phases of rifting, marine incursion,
and open marine conditions, as the northern part of
the South Atlantic Ocean opened.
The rift phase is marked by a thick sequence
of lacustrine deposits of Neocomian age. The contained palynofloras are dominated by Classopollis

Table 2
Relative frequencies (%) of major groups represented in sporepollen assemblages from Albian and Cenomanian sediments of Brazil
Age

Spores

Polyplicates

Classopollis

Elaterates

Angiosperms

Others

Latest Cenomanian
Late Cenomanian
Early Cenomanian
Late Albian
Early Albian

5
5
5
5
15

5
15
30
35
30

3
20
25
30
40

2
10
20
20
3

60
40
15
8
10

25
10
5
2
4

232
R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

Fig. 5. Known palaeogeographic distribution of Elaterates assemblages in mid-Cretaceous strata. Plotted on a mid-Cretaceous (100 Ma; earliest Cenomanian) palaeogeographic map (after Barron et al., 1981). The mid-Cretaceous Elaterates province extended from the low latitude region surrounding the northern part of the proto-South
Atlantic Ocean to southeastern Asia. Oldest reported members of the complex are Elateropollenites jardinei and Pentapsis valdiviae, both of which are restricted to lower
Albian sediments. The former species is known in low frequencies in palynofloras of South America (Venezuela, Peru, Brazil) and Africa (Ivory Coast), and the latter only
from South America. Early diversification of the complex occurred soon after (late early Albian) with appearances of Elaterosporites, Alaticolpites, and Elaterocolpites.
Thereafter diversity and frequency levels increased to an acme at the Albian=Cenomanian boundary, and in Brazil the complex extended south to the Campos Basin, Rio de
Janeiro State. Last appearances of the elaterate complex are in upper Cenomanian sediments. Amongst taxa represented in the Cenomanian are Senegalosporites costatus
(reported here for the first time from Brazil) and S. petrobrasi, which, on present records, are restricted to the Barreirinhas and Araripe basins in Brazil and to Senegal in
Africa.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

ature gradient may have been less than today (Barron

and Washington, 1982). By the close of the Cenomanian temperatures are thought to have lessened with
the onset of deeper and more open marine conditions
as the South Atlantic Ocean widened; at this time
elaterate pollen disappear from the record whereas
angiosperm pollen display rapid diversification (Table 2; Fig. 3).
Relationships between the decline in frequency
and diversity of the ephedroid elaterates and
cheirolepidacean pollen and increased diversity of
the angiosperms have been noted (Brenner, 1963;
Hughes, 1976; Doyle et al., 1977; Doyle et al., 1982;
Crane, 1987; Crane et al., 1995) as indicating profound vegetational changes that heralded the rise to
dominance of the angiosperms in the terrestrial vegetation of low latitudinal regions early in the Late
Cretaceous.
Moreover, the trigger for the rapid spread of
angiosperms may well have resulted from ecological
instability associated with opening of oceans and
fluctuating climates.

Acknowledgements
We thank the Management of Petrobras Research
Center for permission to publish this paper and
Wendy Armstrong, Department of Botany, University of Queensland for expert ultrasectioning and
assistance with Transmission Electron Microscopy.
Helpful reviews from Dr. G.F.W. Herngreen and Dr.
S.K. Srivastava are acknowledged. Support from the
Australian Research Council during the tenure of a
Senior Research Fellowship by MED is gratefully
acknowledged. Mark Schendel (Amoco, Houston)
drafted Figs. 1 and 2.

References
Barron, E.J., Washington, W.M., 1982. Cretaceous climate: a
comparison of atmospheric simulations with the geologic
record. Palaeogeogr., Palaeoclimatol., Palaeoecol. 40, 103133.
Barron, E.J., Harrison, C.G.A., Sloan, J.L., Hay, W.W., 1981.
Paleogeography, 180 m.y. to the present. Eclogae Geol. Helv.
74, 443470.
Boltenhagen, E., 1967. Spores et pollen du Cretace superieur du
Gabon. Pollen Spores 9, 335355.

233

Boltenhagen, E., 1982. Amendement de Sofrepites legouxae Jard.

1967 Pollen Albien du Gabon. Rev. Micropaleontol. 25, 150
153.
Brenner, G.J., 1963. The spores and pollen of the Potomac Group
of Maryland. Md. Dep. Geol. Mines Water Resour. Bull. 27,
1215.
Brenner, G.J., 1968. Middle Cretaceous spores and pollen from
northeastern Peru. Pollen Spores 10, 341383.
Brenner, G.J., 1976. Middle Cretaceous floral provinces and
early migrations of Angiosperms. In: Beck, C.B. (Ed.), Origin
and Early Evolution of Angiosperms. Columbia Univ. Press,
New York, NY, pp. 2347.
Crane, P.R., 1987. Vegetational consequences of the angiosperm
diversification. In: Friis, E.M., Chaloner, W.G., Crane, P.R.
(Eds.), The Origins of Angiosperms and their Biological Consequences. Cambridge Univ. Press, pp. 107144.
Crane, P.R., 1988. Major clades and relationships in the higher
gymnosperms. In: Beck, C.B. (Ed.), Origin and Evolution of
Gymnosperms. Columbia Univ. Press, New York, NY, pp.
218272.
Crane, P.R., 1996. The fossil history of the Gnetales. Int. J. Plant
Sci. 157 (6 Suppl.), S50S57.
Crane, P.R., Friis, E.M., Pedersen, K.R., 1995. The origin and
early diversification of angiosperms. Nature 374, 2733.
Dettmann, M.E., 1963. Upper Mesozoic microfloras from southeastern Australia. Proc. R. Soc. Victoria 77, 1148.
Doyle, J.A., Biens, P., Doerenkamp, A., Jardine, S., 1977.
Angiosperm pollen from the pre-Albian Lower Cretaceous
of Equatorial Africa. Bull. Cent. Rech. Explor.-Prod. ElfAquitaine 1, 451473.
Doyle, J.A., Jardine, S., Doerenkamp, A., 1982. Afropollis, a
new genus of early angiosperm pollen, with notes on the Cretaceous palynostratigraphy and paleoenvironments of northern
Gondwana. Bull. Cent. Rech. Explor.-Prod. Elf-Aquitaine 6,
39117.
El-Ghazaly, G., Rowley, J.R., 1997. Pollen wall of Ephedra
foliata. Palynology 21, 718.
Elsik, W.C., 1974. Fossil auriculate pollen. Pollen Spores 16,
507534.
Gregory, W.A., Hart, G.F., 1992. Towards a predictive model for
the palynologic response to sea-level changes. Palaios 7, 333.
Herngreen, G.F.W., 1973a. Palynomorphes du Cretace moyen du
Nord-Est du Bresil. Resultats de lanalyse palynologique de
quelques sondages et comparaisons avec lAfrique. Symposium Palynologie et Derive des Continents, Association des
Palynologues de Langue Francaise, Strasbourg, October 1973,
pp. 1314 (abstract).
Herngreen, G.F.W., 1973b. Palynology of AlbianCenomanian
strata of borehole 1-QS-1-MA, State of Maranhao, Brazil.
Pollen Spores 15, 515555.
Herngreen, G.F.W., 1974. Middle Cretaceous palynomorphs from
northeastern Brazil. Results of a palynological study of some
boreholes and comparison with Africa and the Middle East.
Sci. Geol. Bull. 27, 101116.
Herngreen, G.F.W., 1975a. An Upper Senonian pollen assemblage of borehole 3-PIA-10-Al, State of Alagoas, Brazil.
Pollen Spores 17, 93140.

234

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

Herngreen, G.F.W., 1975b. Palynology of Middle and Upper

Cretaceous strata in Brazil. Meded. Rijks Geol. Dienst N. S.
26, 3991.
Herngreen, G.F.W., Chlonova, A.F., 1981. Cretaceous microfloral
provinces. Pollen Spores 23, 441555.
Herngreen, G.F.W., Kedves, M., Rovina, L.V., Smirnova, S.B.,
1996. Cretaceous floral provinces: a review. In: Jansonius, J.,
McGregor D.C. (Eds.), Palynology: Principles and Applications. Am. Assoc. Stratigr. Palynol. Found. 3, 11571188.
Horowitz, A., 1970. Jurassic microflora from the northern Negev,
Israel. Isr. J. Earth Sci. 19, 153182.
Hughes, N.F., 1976. Palaeobiology of Angiosperm Origins, Problems of Mesozoic Seed-plant Evolution. (Cambridge Earth
Science Series.) Cambridge Univ. Press, 242 pp.
ICBN (International Code of Botanical Nomenclature), 1994.
Tokyo Code. In: Greuter, W., Chaloner, W.G., Demoulin, V.,
Grolle, R., Hawksworth, D.L., Nicolson, D.H., Silva, P.C.,
Stafleu, F.A., Voss, E.G. (Eds.), Adopted by the Fifteenth
International Botanical Congress; Regnum Vegetabile, 131,
International Association of Plant Taxonomy. Koeltz, Konigstein, 389 pp.
Jaillard, E., Ordonez, M., Huaman, C., Jimenez, N., Rivadeneira,
M., Zambrano, I., 1994. Sintesis estratigrafica del Cretaceo
y Paleogeno de la Cuenca Oriental del Ecuador. Informe del
Convenio ORSTOM-Petroproduccion, Deciembre 1994, 136
pp.
Jansonius, J., Hills, L.V., 19761996. Genera File of Fossil
Spores and Pollen. Dep. Geol., Univ. Calgary, Spec. Publ.
Jardine, S., 1967. Spores a` expansions en forme delate`res du
Cretace moyen dAfrique occidentale. Rev. Palaeobot. Palynol.
1, 235258.
Jardine, S., Magloire, L., 1965. Palynologie et stratigraphie du
Cretace des bassins du Senegal et de Cote dIvoire. In: Colloque de Micropaleontologie, Dakar, 1963. Mem. Bur. Rech.
Geol. Min. 32, 187245.
Jardine, S., Doerenkamp, A., Legoux, O., 1972. Le genre Hexaporotricolpites Boltenhagen 1967: morphologie, systematique,
stratigraphie et extension geographique. In: Proceedings Colloque African Micropaleontologie Abdjan, 1970, 4, 175191.
Jardine, S., Biens, P., Doerenkamp, A., 1974a. Dicheiropollis etruscus, un pollen caracteristique du Cretace inferieur
afro-sudamericain. Consequences pour levaluation des unites
climatiques et implications dans la derive des continents. In:
Palynologie et Derive des Continents. Sci. Geol. Bull. Strasbourg 27, 87100.
Jardine, S., Kieser, G., Reyre, Y., 1974. Lindividualisation progressive du continent africain vue a` travers les donnees palynologiques de lEre Secondaire. In: Palynologie et Derive des
Continents. Sci. Geol. Bull. Strasbourg 27, 6985.
Jingxian, Y., 1981. Late Cretaceous sporo-pollen assemblages of
Shache District, Xinjiang. Acta Geol. Sin. 2, 93104.
Kurman, M.H., Zavada, M.S., 1994. Pollen morphological diversity in extant and fossil gymnosperms. In: Kurman, M.H.,
Doyle, J.A. (Eds.), Ultrastructure of Fossil Spores and Pollen.
Royal Botanic Gardens, Kew, pp. 123137.
Lammons, J.M., 1970. Pentapsis, a new palynomorph genus

from the Cretaceous (Aptian) of Peru. Micropaleontology 16,

175178.
Lima, M.R., 1978. Palynological characteristics of the Albian
in Brazil. Advances in Palaeobotany and Allied Sciences in
Brazil. Bol. Inst. Geocienc. Univ. Sao Paulo 9, 140143.
Lima, M.R., 1980. Palinologia da Formacao Santana (Cretaceo
do Nordeste do Brasil). III Descricao sistematica dos polens
da Turma Plicates (Subturma Costates). Ameghiniana 17, 14
47.
Milne, L.A., 1994. Relationship between Propylipollis annularis
(Tertiary dispersed pollen) and extant Xylomelum (Proteaceae).
In: Kurmann, M.H., Doyle, J.A. (Eds.), Ultrastructure of Fossil
Spores and Pollen. Royal Botanic Gardens, Kew, pp. 193213.
Milne, L.A., 1998. Surface embedding of fossil pollen for timeand cost-effective ultramicrotomy (TEM) and microscopy
(LM, SEM, TEM) of single grains. In: Bryant Jr., V.M.,
Wrenn, J.H. (Eds.), New Developments in Palynomorph Sampling, Extraction, and Analysis. Am. Assoc. Stratigr. Palynol
Contrib. Ser. 33, 95105.
Muller, H., 1966. Palynological investigations of Cretaceous sediments in northeastern Brazil. In: Van Hinte, J.E. (Ed.), Proc.
2nd. W. Afr. Micropaleontol., Colloq., Ibadan, 1965, 2: 123136.
Osborn, J.M., Taylor, T.N., Lima, M.R., 1993. The ultrastructure
of fossil ephedroid pollen with gnetalean affinities from the
Lower Cretaceous of Brazil. Rev. Palaeobot. Palynol. 77, 171
184.
Phipps, D., Playford, G., 1984. Laboratory techniques for extraction of palynomorphs from sediments. Pap. Dep. Geol. Univ.
Queensl. 11, 123.
Pocock, S.A.J., Vasanthy, G., 1988. Cornetipollis reticulata, a
new pollen with angiospermid features from Upper Triassic
(Carnian) sediments of Arizona (U.S.A.), with notes on Equisetosporites. Rev. Palaeobot. Palynol. 55, 337356.
Regali, M.S.P., 1989. Sistematica, bioestratigrafia e paleogeografia do genero Elateropollenites Herngreen 1973, na
margem equatorial brasileira. Bol. Inst. Geocienc.-USP Sao
Paulo Publ. Espec. 7, 45153.
Regali, M.S.P., Viana, C.F., 1989. Late JurassicEarly Cretaceous in Brazilian Sedimentary Basins: Correlation with the
Internacional Standard Scale. PETROBRAS=SEDES, Rio de
Janeiro, pp. 4795.
Regali, M.S.P., Uesugui, N., Santos, A.S., 1975a. Palinologia dos
sedimentos meso-cenozoicos do Brazil (I). Bol. Tec. Petrobras
17, 177191.
Regali, M.S.P., Uesugui, N., Santos, A.S., 1975b. Palinologia
dos sedimentos meso-cenozoicos do Brazil (II). Bol. Tec.
Petrobras 17, 263301.
Rowley, J.R., 1996. Exine origin, development and structure in
pteridophytes, gymnosperms and angiosperms. In: Jansonius,
J., McGregor, D.C. (Eds.), Palynology: Principles and Applications. Am. Assoc. Stratigr. Palynol. Found. 1, 443462.
Schrank, E., Ibrahim, M.I.A., 1995. Cretaceous (Aptian
Maastrichtian) palynology of foraminifera-dated wells
(KRM-1, AG-18) in northwestern Egypt. Berl. Geowiss. Abh.
Reihe A 177, 144.

R. Dino et al. / Review of Palaeobotany and Palynology 105 (1999) 201235

Srivastava, S.K., 1978. Cretaceous spore-pollen floras. Biol.
Mem. Palaeopalynol. Ser. 53, 1130.
Srivastava, S.K., 1981. Evolution of Upper Cretaceous phytogeographic provinces and their pollen flora. Rev. Palaeobot.
Palynol. 35, 155173.
Srivastava, S.K., 1984. A new elater-bearing Late Albian pollen
species from offshore eastern Saudi Arabia. Bot. J. Linn. Soc.
89, 231238.
Srivastava, S.K., 1994. Evolution of Cretaceous phytogeoprovinces, continents and climates. Rev. Palaeobot. Palynol.
82, 197224.
Stover, L.E., 1963. Some Middle Cretaceous palynomorphs from
West Africa. Micropaleontology 9, 8594.
Trevisan, L., 1980. Ultrastructural notes and considerations on
Ephedripites, Eucommiidites and Monosulcites pollen grains
from Lower Cretaceous sediments of southern Tuscany (Italy).
Pollen Spores 22, 85132.
Vakhrameev, V.A., 1978. The climates of the northern hemi-

235

sphere in the Cretaceous in the light of palaeobotanical data.

Paleontol. J. 2, 317.
Van Campo, M., Lugardon, B., 1973. Structure grenue infratectale de lectexine des pollens de quelques Gymnospermes et
Angiospermes. Pollen Spores 15, 171188.
Wood, G.D., Gabriel, A.M., Lawson, J.C., 1996. Palynological
techniques processing and microscopy. In: Jansonius, J.,
McGregor, D.C. (Eds.), Palynology: Principles and Applications. Am. Assoc. Stratigr. Palynol. Found. 1, 2950.
Zavada, M.S., 1984. Angiosperm origins and evolution based on
dispersed fossil pollen ultrastructure. Ann. Mo. Bot. Gard. 71,
444463.
Zavada, M.S., 1990. The ultrastructure of three monosulcate
pollen grains from the Triassic Chinle Formation, western
United States. Palynology 14, 4151.
Zhang, Y., Zhan, J., 1986. Evolution of angiosperm pollen of
the early Late Cretaceous in the Western Tarim Basin, south
Xinjiang. Acta Palaeobot. Palynol. Sin. 1, 4763.