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A quantitative review of the lifestyle, habitat and trophic diversity of

dinoflagellates (Dinoflagellata, Alveolata)

Article  in  Systematics and Biodiversity · September 2012

DOI: 10.1080/14772000.2012.721021

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 Systematics and Biodiversity (2012), 10(3): 267–275

Perspective
A quantitative review of the lifestyle, habitat and trophic diversity
of dinoflagellates (Dinoflagellata, Alveolata)

FERNANDO GÓMEZ
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

Instituto Cavanilles de Biodiversidad y Biologı́a Evolutiva, Universidad de Valencia, PO Box 22085, 46071 Valencia, Spain
(Received 16 June 2012; revised 8 August 2012; accepted 9 August 2012)

This study reviews the trends in the lifestyle, habitat distribution and trophic diversity of the 2377 described species of
dinoflagellates (Dinophyceae). Most of the dinoflagellates inhabit marine waters, whereas 17% of the total species have
colonized continental waters. Dinoflagellates are dominated by planktonic species, while benthic forms represented 8% of
the species. From the total number of species, 49% are heterotrophic (devoid of plastids), while 51% of the species have
been reported with plastids (that does not strictly imply autotrophy). All the basal dinoflagellates (ellobiopsids,
Duboscquodinida, Syndiniales) are heterotrophic, with the exception of a few Noctilucales (Spatulodinium). The
continental waters are highly dominated by plastid-containing species (88%), while in marine environments there is a slight
dominance of heterotrophic species (58%). Most of the dinoflagellates are free-living forms; only 7% of the total species
are parasites. The dinokaryotic parasites appear in separate clades, and about 40% of them contain plastids. The beneficial
or mutualistic symbionts (21 species, 1%) are photosynthetic species dispersed into at least three clades.
Key words: benthic, biodiversity, Dinophyceae, freshwater Dinophyta, heterotrophy, parasite, symbioses, syndineans

Introduction reefs, one of the most diverse ecosystems on Earth (Trench,

The dinoflagellates are an important group of protists in 1993; LaJeunesse, 2002).
marine and freshwaters. Their adaptation to a wide range Dinoflagellates show a high versatility in the habitat
of environments is reflected by tremendous morphologi- distribution, marine or continental waters, and adaptation
cal and trophic diversity (Taylor, 1987). Like their alveo- to pelagic or benthic environments. They also show a high
late relatives, apicomplexans and ciliates, the dinoflagellate trophic diversity (reviewed by Gaines & Elbrächter, 1987;
cortex has a set of flattened vesicles referred to as alveoli. Stoecker, 1999; Hansen, 2011). However, no review has
Dinoflagellates possess a ribbon-like transverse flagellum ever reported the precise number of species associated
encircling the cell and another longitudinal flagellum. For with each type of habitat, lifestyle or trophic diversity.
the dinoflagellate core, the nucleus, dinokaryon, contains This analysis reviews these general trends based on data
large amounts of DNA and unique cytological features such of each dinoflagellate species. The aim of this study was to
as permanently condensed chromosomes and a lack of typi- provide a general view of the habitat distribution, lifestyle
cal eukaryotic histones (Spector, 1984; Lin, 2011). Among and trophic diversity, using quantitative data of the whole
the basal dinoflagellates, the syndinian nucleus is much dinoflagellate group.
closer to the eukaryotic type. Dinoflagellates are both pri-
mary producers and consumers in the food web, sometimes
at the same time, and best known for their dominant role in Materials and methods
causing harmful algal blooms. Furthermore, dinoflagellates The primary source for analysis is the checklist of living
can be either ecto- or endoparasites (Chatton, 1920; Cachon dinoflagellates by Gómez (2012) that listed 2377 described
& Cachon, 1987; Coats, 1999). As mutualistic symbionts, species. The information on each species has been labelled
dinoflagellates provide essential nutrients to most corals according to its habitat distribution (marine or continental,
and numerous other marine invertebrates, supporting coral and planktonic or benthic), lifestyle (free-living, parasitic or
mutualistic symbiont), and trophic diversity (heterotrophic
Correspondence to: Fernando Gómez. E-mail: fernando.gomez@ and plastid-containing). The database is provided (Table
fitoplancton.com S1, see supplementary material, which is available on the

ISSN 1477-2000 print / 1478-0933 online

C 2012 The Natural History Museum
http://dx.doi.org/10.1080/14772000.2012.721021
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

268
F. Gómez
 Lifestyle, habitat and trophic diversity of dinoflagellates 269

Supplementary tab of the article’s Taylor & Francis Online of chlorophyll and plastids. It is difficult to establish whether
page at http://dx.doi/10.1080/14772000.2012.721021). the plastids are sustaining the cell independently, since other
However, information on a precise species should be sources of carbon, and most photosynthetic species relied
verified in the specific literature. on exogenous vitamins (Tang et al., 2010). It has long
There are no examples of dinoflagellate species which been recognized that some photosynthetic dinoflagellates
are able to proliferate in both marine and oligohaline con- have food vacuoles and feed on other protists (Stoecker,
tinental waters. However, the distinction for marine or con- 1999; Jeong et al., 2005; Hansen, 2011). For some di-
tinental species may be difficult for some species described noflagellates, it is not clear whether their photosynthetic
from estuarine or coastal brackish waters subjected to strong machinery is either their own or derived from prey, nor
fluctuations in salinity. At these locations, continental and is it clear whether the plastids or endosymbionts need to
marine species may co-exist. Species described from estuar- be periodically replenished through ingestion (e.g. Dino-
ies and brackish coastal environments (Kryptoperidinium, physis, Garcı́a-Cuetos et al., 2010; Pfiesteria, Feinstein
Oxyrrhis, Pfiesteria) are labelled as marine species. Other et al., 2002). The species devoid of plastids or pigments
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

habitat distribution concerns the species living in the water are labelled as ‘heterotrophic’. It is more difficult to find
column (plankton) or associated with the bottom (benthic). a term for the species that possess plastids (auxotrophic,
This distinction is not clear-cut because the turbulence may autotrophic, mixotrophic, photosynthetic). Thus, the rest of
re-suspend the benthic species (tychoplankton), and plank- the taxa are pooled as ‘plastid-containing’ species. Many
tonic species have benthic life stages (e.g. cysts). In the case of the original species descriptions did not specify the pres-
of the parasites, they are considered planktonic or benthic ence or absence of chloroplasts, or in some cases the food
according to the habitat of their hosts, although the infecting contents were misinterpreted as plastids. This distinction is
dinospores disperse in the water column. subjected to the difficulties to determine the trophic char-
The lifestyle of dinoflagellates is divided into free-living acter of numerous species.
and symbiotic species. The latter are divided into mutual-
istic symbionts (i.e. both organisms benefit), and parasites Results
(the dinoflagellate benefits at the expense of the host). The
distinction between parasitic and heterotrophic dinoflag- Trends in habitat distribution
ellate is not immediate. Parasitic dinoflagellates are con- The dinoflagellates have reached high morphological di-
sidered those forms that have morphologically different versity (Fig. 1) and show higher species richness in marine
feeding and reproductive stages and that produce more environments. From the total of 2377 described species of
than two daughter cells after each feeding event (Gaines & dinoflagellates, 1957 species (82%) were described from
Elbrächter, 1987). The dinoflagellates are considered mu- marine waters (including estuaries and brackish coastal
tualistic symbionts when the dinoflagellate is smaller than environments) (Figs 2–17). Most of the marine dinoflag-
the host as occurred in corals, various types of anemones, ellates were free-living and marine parasites encompassed
jellyfish and molluscs of the reef, and in planktonic Acan- 137 species (Fig. 3). All the described dinoflagellates living
tharia, Foraminifera and Radiolaria (Spero & Angel, 1991). in beneficial symbiotic consortia were marine (21 species,
In other cases, the dinoflagellate is larger than the sym- 1%). Marine dinoflagellates are dominated by planktonic
biont and it acts as a host (as has occurred in some species (1787 species, 91%), with 170 benthic species
dinoflagellate–cyanobacteria consortia). This is not consid- (9%) (Fig. 16). The number of heterotrophic species in
ered a symbiotic or parasitic relationship, and the dinoflag- marine environments was slightly higher (1131 species,
ellates are labelled as free-living heterotrophic species. 58%) than for plastid-containing species (Table S2, see
Dinoflagellates have been traditionally categorized as au- supplementary material, which is available on the Sup-
totrophic or heterotrophic, based on the presence or absence plementary tab of the article’s Taylor & Francis Online

←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−
Fig. 1. Diversity of major lineages of dinoflagellates: 1. Ellobiopsis; 2. Oxyrrhis; 3. Duboscquella; 4. Syndinium; 5. Kofoidinium;
6. Noctiluca; 7. Spatulodinium; 8. Scaphodinium; 9. Haplozoon; 10. Crypthecodinium; 11. Dinothrix; 12. Peridinium quinquecorne;
13. Durinskia; 14. Phytodinium; 15. Cystodinium; 16. Borghiella; 17. Sphaerodinium; 18. Biecheleria. 19. Symbiodinium; 20. Takayama;
21. Karlodinium; 22. Brachidinium; 23. Pseliodinium: 24. Torodinium; 25. Gynogonadinium; 26. Amphidinium; 27. Gymnodinium;
28. Polykrikos; 29. Warnowia; 30. Erythropsidinium; 31. Dissodinium; 32. Chytriodinium; 33. Prorocentrum s.s.; 34. Dinophysis;
35. Citharistes; 36. Histioneis; 37. Parahistioneis; 38. Ornithocercus; 39. Phalacroma; 40. Amphisolenia; 41. Triposolenia; 42.
Sinophysis; 43. Exuviaella/Haplodinium; 44. Peridinium s.s.; 45. Protoperidinium s.s.; 46. Diplopsalis; 47. Thecadinium; 48. Gonyaulax;
49. Spiraulax; 50. Lingulodinium; 51. Amylax; 52. Goniodoma; 53. Gambierdiscus; 54. Ostreopsis; 55. Coolia; 56. Alexandrium; 57.
Pyrodinium; 58. Centrodinium; 59. Fragilidium; 60. Pyrophacus; 61. Pyrocystis; 62. Ceratium; 63. Neoceratium; 64. Ceratocorys; 65.
Protoceratium; 66. Schuettiella; 67. Blastodinium; 68. Heterocapsa; 69. Amphidiniopsis; 70. Herdmania; 71. Archaeperidinium; 72.
Podolampas; 73. Blepharocysta; 74. Roscoffia; 75. Lessardia; 76. Heterodinium; 77. Corythodinium; 78. Gyrodinium; 79. Hemidinium;
80. Glenodinium; 81. Pfiesteria; 82. Scrippsiella; 83. Oodinium.
 270 F. Gómez

2 3 4 5
TAL
IN EN
PARASITE NT
PLASTID- HETERO- FREE- CO BENTHIC
CONTAINING TROPHIC LIVING SYMBIOSIS

MARINE PLANKTON

PA SYM

CONTINENTAL
R
6 PARASITE
7 8 HET 9
HETERO-
HETERO- HET
TROPHIC

PARASITE
HETERO-
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TROPHIC

BENTHIC
HET TROPHIC CHL
CHL
FREE- FREE-
LIVING LIVING PLASTID- PLASTID-
FREE PLASTID-
CONTAINING CONTAINING
CONTAINING
FREE-LIVING MARINE PLANKTON

heterotrophic

CONTINENTAL
plastid-

SITE
10 CONTINENTAL
11 12 SYM
13

PARA
CONTINENTAL E
IT
CONTINENTAL
RAS

BENTHIC
FREE- PA
PARASITE

MARINE LIVING
FREE- FRE
MARINE FREE- PAR
LIVING
MARINE LIVING
MARINE
FREE-LIVING MARINE PLANKTON

plastid- heterotrophic

CONTINENTAL
N

BENTHIC BENTHIC BENTHIC

14 15 16 17
BE

L
TA
BENTHIC EN
N TIN CON
PARASITE

CO

BENTHIC
PLANKTON
PLK MAR
PLANKTON PLANKTON
PLANKTON PLANKTON MARINE
FREE-LIVING MARINE PLANKTON

plastid- heterotrophic

Figs 2–17. Pie charts of the percent of dinoflagellates (n = 2377 species) according to the trophic classification (heterotrophic or plastid-
containing species), lifestyle (free-living species, parasites or mutualist symbionts) and habitat (marine or continental, planktonic or
benthic). CHL: plastid-containing species; HET: heterotrophic; FRE: free-living; PAR: parasites; SYM: mutualistic symbionts; MAR:
marine; CON: species living in continental waters; PLK: planktonic, living in the water column; BEN: benthic, living in the benthos.

page at http://dx.doi/10.1080/14772000.2012.721021). All freshwater species were benthic (30 species, 7%), mainly
the basal dinoflagellates have been described from ma- composed of a group of insufficiently known taxa represent-
rine waters. Among the Dinokaryota, the order Dino- ing the genera, Cystodinium, Stylodinium and Tetradinium.
physales is exclusively composed of marine species, In contrast to the marine species, the continental species
and Prorocentrales and Gonyaulacales were highly dom- were highly dominated by plastid-containing species (88%)
inated by marine species (Table S1, see supplemen- (Fig. 8). The few heterotrophic species (48 species, 11%)
tary material, which is available on the Supplementary were little-known species of the genera Gymnodinium,
tab of the article’s Taylor & Francis Online page at Gyrodinium, Katodinium or Stylodinium. The percentage
http://dx.doi/10.1080/14772000.2012.721021). of parasitic species in continental waters (27 species,
A total of 420 species have been described from 6%) was slightly lower than in marine waters (Fig. 12).
continental waters (17% of 2377 species) (Fig. 4). A few Several genera of continental parasites contained plastids
 Lifestyle, habitat and trophic diversity of dinoflagellates 271

(Cystodinium, Crepidoodinium) and others were devoid of Trends in trophism

plastids (Cystodinedria, Oodinioides and Stylodinium). The heterotrophic species constituted 49% of the to-
Concerning the distribution of dinoflagellates in the tal species (1179 species) (Fig. 2). They slightly dom-
water column, most were planktonic (2177, 91%) (Fig. 5). inate in marine waters, while the proportion was low
These planktonic species were preferentially marine (1787, in continental waters with only 48 heterotrophic species.
91%), and about one half contained plastids (Fig. 9). A total Most of the parasites were heterotrophic (130/164 species)
of 127 (5%) species were parasites. There were 200 species (Fig. 6), and about 30% of the benthic species were het-
described from benthic environments (8% of total), mainly erotrophic (67/200 species) (Fig. 14). All the basal di-
algal epiphytes or sand-dwelling species (episammic). noflagellates were heterotrophs, with the exception of
Most of the benthic species were marine (170 species, 85%) a life stage of Spatulodinium, known as Gymnodinium
and plastid-containing (133 species, 66%) (Table S2, see lebouriae that contained plastids (Table S1, see supple-
supplementary material, which is available on the Supple- mentary material, which is available on the Supplemen-
mentary tab of the article’s Taylor & Francis Online page tary tab of the article’s Taylor & Francis Online page at
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

at http://dx.doi/10.1080/14772000.2012.721021). Benthic http://dx.doi/10.1080/14772000.2012.721021). Among the

species have not been described among basal dinoflagel- 2280 dinokaryotic dinoflagellates, 1083 species (48%) are
lates, with the exception of Hematodinium, which para- heterotrophs. None of the classical major orders (Peri-
sitizes benthic crustaceans. Among the dinokaryonts, the diniales, Gymnodiniales, Prorocentrales, Dinophysales,
order Gonyaulacales showed a high proportion of benthic Gonyaulacales) is exclusively constituted of heterotrophic
species due to the epiphytic genera, Coolia, Gambierdiscus, species. Most of Dinophysales were heterotrophic, with the
Ostreopsis and the sand-dwelling Thecadinium. The per- exception of some Dinophysis and a few Phalacroma. Sev-
centage of benthic parasitic species (37 species, 18%) was eral families of Peridiniales sensu lato were exclusively
higher than for the planktonic species. The benthic parasites heterotrophic species such as Amphidiniopsidaceae, Het-
belonged to the heterotrophic genera, Haplozoon and Stylo- erodiniaceae, Podolampadaceae and Protoperidiniaceae. In
dinium, and the plastid-containing Cystodinium. Among the contrast, the orders Brachidiniales and Prorocentrales were
beneficial symbiotic species, Symbiodinium spp. and Am- exclusively composed of plastid-containing species, as well
phidinium belauense are associated with benthic organisms as the families Dinotrichaceae, Glenodiniaceae, Heterocap-
(Table S1, see supplementary material, which is available on saceae, Peridiniaceae sensu stricto and Symbiodiniaceae
the Supplementary tab of the article’s Taylor & Francis On- (Table S1, see supplementary material, which is available on
line page at http://dx.doi/10.1080/14772000.2012.721021). the Supplementary tab of the article’s Taylor & Francis On-
line page at http://dx.doi/10.1080/14772000.2012.721021).
Trends in the lifestyle
The dinoflagellates are dominated by free-living species
(2192 species, 92%) of which 1143 or 52% are plastid- Discussion
containing species (Figs 3, 7). A total of 164 dinoflagellates
species (6.8%) were parasites. About one half of the para- Trends in the habitat distribution
sites were basal dinoflagellates (77 species), and 87 species Most major microbial lineages originated in ancient oceans
were dinokaryotic parasites. Most of the parasites were het- (e.g. Cavalier-Smith, 2006). Dinoflagellates show a higher
erotrophs, with the exceptions of 34 species that contained species richness in marine environments (four of each five
plastids. The main representatives of the plastid-containing species). Bourrelly (1970) and Taylor (1987, p. 409) re-
parasites were Blastodinium, a parasite of marine cope- ported that approximately only 220 species inhabit fresh-
pods, Crepidoodinium and Piscinoodinium, parasites of water environments. This study listed 420 species living
freshwater fishes, and the insufficiently known species of in continental waters. The proportion of marine species
Cystodinium, a parasite of freshwater algae (Table S1, could be higher because: (1) for species descriptions, the
see supplementary material, which is available on the Sup- continental waters have been historically more investigated
plementary tab of the article’s Taylor & Francis Online page than the oceans; (2) it could be an excess of species de-
at http://dx.doi/10.1080/14772000.2012.721021). scribed for several freshwater genera such as Cystodinium,
There were 21 species of dinoflagellates living in Hemidinium or Tetradinium because they may correspond
a mutually endosymbiotic association. The genus Sym- to life stages of other known species (i.e. Baumeister, 1957;
biodinium with 15 species and one species of Pelago- Skvortzov, 1968), as well as many insufficiently known
dinium (family Symbiodinium) constituted the main freshwater species of Amphidinium and Gymnodinium;
clade of mutualist symbionts (Table S1, see supplemen- and (3) environmental sequencing of the deep open ocean
tary material, which is available on the Supplementary or deep sediments revealed numerous novel heterotrophic
tab of the article’s Taylor & Francis Online page at clades dinoflagellates, that have not been morphologically
http://dx.doi/10.1080/14772000.2012.721021). characterized (López-Garcı́a et al., 2001, 2007). They are
 272 F. Gómez

often in smaller size fractions (<5 µm) that are difficult to Little-known freshwater genera, with an apparent excess
examine and differentiate by classical methods. of species (Cystodinium, Stylodinium and Tetradinium),
Several species of dinoflagellates are adapted to high may reduce the proportion of benthic species in continental
fluctuations of salinity (e.g. Oxyrrhis). However, no species waters. Many of these species are parasites of benthic
is able to proliferate in both oligohaline and marine waters. hosts. They are not highly flattened as typical in benthic
Logares et al. (2007) concluded that marine and freshwa- dinoflagellates. Only three species of Prorocentrum (=
ter dinoflagellates are usually not closely related, several ?Haplodinium antjoliense) and Amphidiniopsis sibbaldii
freshwater species cluster into monophyletic groups, only showed flattened morphologies in freshwater environments.
a small fraction of the marine lineages seem to have colo- Historically, the benthic dinoflagellates have received
nized freshwaters, and most marine–freshwater transitions less attention than the pelagic species. Beyond a few pi-
do not seem to have occurred recently. oneer studies (Herdman, 1924; Balech, 1956), the ben-
As an example, the type species of the specious genus thic species have been undersampled for decades. A high
Gymnodinium is a photosynthetic freshwater species. The number of marine benthic species have been described in
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

support for the divergence between marine and continen- the last 20 years, especially species associated with the
tal species of Gymnodinium increases in more complete ciguatera in tropical waters (Coolia, Gambierdiscus, Os-
phylogenetic trees, including the families Chytriodiniaceae treopsis, Prorocentrum). The sampling coverage of benthic
and Warnowiaceae (Gómez et al., 2009a, 2009c). Genera species is nearly restricted to shallow waters as epiphytes of
such as Amphidiniopsis, Gyrodinium or Prorocentrum con- macrophytes, coral reefs or sandy beaches. Environmental
tain both marine and freshwater species. However, in some sequencing libraries revealed that there may be consider-
cases, such as Gyrodinium, the addition of more species se- ably high diversity of undescribed heterotrophic or parasitic
quences into the molecular phylogenies could support the species yet to be described in the deep ocean floor (Moreira
generic separation of marine and freshwater species. The & López-Garcı́a, 2003).
molecular phylogeny of the marine and freshwater species
supports the generic separation of Ceratium (Gómez et al.,
2010a). The marine species, Neoceratium, reaches a high Trends in lifestyle
speciation, while the freshwater Ceratium is restricted to a Most of the dinoflagellates were free-living species (92%
few species. of 2377). In contrast, the closest relatives to the dinoflag-
The present study reveals that continental waters showed ellates, apicomplexans and perkinsids, and nearly all the
a high percentage of plastid-containing species (88%). basal dinoflagellates are parasites (Zhang et al., 2011).
Dinoflagellates have a lower photosynthetic efficiency Cachon & Cachon (1987) listed 66 parasitic dinoflag-
than other protist groups (Morse et al., 1995; Tang, 1996). ellates, and Drebes (1984) estimated about 140 species.
This may constitute a disadvantage to proliferate in the Taylor et al. (2008) estimated parasites were 5% of the total
oligotrophic open ocean. In contrast, the higher nutrient species. The present study reported 164 species of para-
concentrations in the continental waters may favour sites (7% of the total 2377 species). About one half of the
the development of plastid-containing dinoflagellates. total species (77 species) belong to the non-dinokaryotic
Dinoflagellates possess the most diverse array of plastids basal dinoflagellates (ellobiopsids, Duboscquodinida, Syn-
of any eukaryotic lineage (Saldarriaga et al., 2001; Hackett diniales). In the molecular phylogenies, a few free-living
et al., 2004). However, the pigment composition of the species branched among the basal dinoflagellates (Oxyrrhis
continental species is less diverse than for the marine ones. and Noctilucales) (Saldarriaga et al., 2003; Gómez et al.,
Common freshwater genera such as Peridinium or Gymno- 2010b). Oxyrrhis is a free-living species that only prolif-
dinium contain the most typical chloroplast of dinoflagel- erates in brackish environments, often associated with the
lates, which is bounded by three membranes and possess unialgal blooms (Dunaliella). The morphology of Oxyrrhis
chlorophylls a and c2 as well as peridinin as a major acces- resembles the dispersive spores of Syndiniales (Chatton,
sory pigment. A few freshwater dinoflagellates, as well as 1920; Skovgaard et al., 2005).
marine species, have a blue pigment, phycobilin, obtained To date, environmental sequences of Duboscquodinida
from a cryptophyte endosymbiont (Yamaguchi et al., 2011). (Marine Alveolate Group I) and Syndiniales (Marine Alve-
Most of the dinoflagellates are planktonic in marine olate Group II) have been retrieved exclusively from marine
and continental ecosystems. Taylor et al. (2008, p. 408) environments (Guillou et al., 2008). Syndiniales are geneti-
estimated 160 marine benthic species, and they reported cally more diverse than Duboscquodinida, and the diversity
that only one explicitly freshwater benthic species has been in the deep-ocean and deep floor is greatly underestimated,
described. From the 200 species of benthic dinoflagellates, because there are more clades than known species (Guillou
85% inhabit marine and 15% continental waters (Figs 2–17, et al., 2008). All the ellobiopsids were described from
Table S2, see supplementary material, which is available on marine waters (Gómez et al., 2009b), although infections
the Supplementary tab of the article’s Taylor & Francis On- by ellobiopsid parasites have been reported in freshwater
line page at http://dx.doi/10.1080/14772000.2012.721021). crustaceans (Bridgeman et al., 2000; Manca et al., 2004).
 Lifestyle, habitat and trophic diversity of dinoflagellates 273

The basal dinoflagellates are considerably dominated by Amphidinium, Aureodinium, Gloeodinium, Gymnodinium,
parasites, while the proportion of parasites is low (3%) Gyrodinium, Prorocentrum, Pyrocystis and Scrippsiella
among the typical dinoflagellates. The parasitism in di- (Spero & Angel, 1991). However, the precise identification
nokaryotes is restricted to 87 species which were often of many of these species and its interpretation as mutualist
dispersed among free-living species. Haplozoon is a para- symbionts is doubtful. The molecular phylogenies support
site with a basal position in the dinokaryotic core (Cachon the polyphyletic origin of dinoflagellate-invertebrate
& Cachon, 1987). However, the other clades of parasitic symbiosis (McNally et al., 1994). Mutualist symbionts
dinoflagellates (Chytriodiniaceae, Oodiniaceae, Piscinood- are separated into at least three clades (Table S1, see
inium) emerge among free-living forms, and suggest that supplementary material, which is available on the Sup-
parasitism is a recent acquisition. So far, the parasitic basal plementary tab of the article’s Taylor & Francis Online
dinoflagellates do not contain plastids, while about 40% page at http://dx.doi/10.1080/14772000.2012.721021). In
of the dinokaryotic parasites contain plastids. Nearly all addition to Symbiodinium, the family Symbiodiniaceae,
the species of Blastodinium contain plastids, although the contain numerous free-living species, and Piscinoodinium,
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

photosynthesis partially covers the cell requirements and a plastid-containing species that is parasitic on freshwater
the rest being ensured by the assimilation of host diges- fishes, and the symbionts of planktonic foraminifera
tive substances (Pasternak et al., 1984). The parasites of Pelagodinium (formerly Gymnodinium) (Siano et al.,
the family Chytriodiniaceae (Chytriodinium, Dissodinium) 2010). The family Endodiniaceae, including Endodinium,
emerged among clades of photosynthetic species of Gymno- have reported under the genera Amphidinium, Gloeo-
dinium. The parasite of copepod eggs, Dissodinium pseu- dinium, Scrippsiella and Zooxanthella (Spero & Angel,
dolunula, possesses plastids, while its closer relatives are 1991). A third clade is composed of a single species,
heterotrophic species (Gómez et al., 2009c). This suggests Amphidinium belauense, living in a flatworm, closely re-
a recent loss of the plastids in Chytriodiniaceae, more than lated to free-living photosynthetic species of Amphidinium
a recent acquisition in D. pseudolunula. The presence of sensu stricto (McNally et al., 1994).
plastids seems to be a reminiscent of its photosynthetic Dinoflagellates show a high proclivity for endosymbio-
ancestor in Dissodinium and Blastodinium, the latter with sis, which is largely reported for plastids (Saldarriaga et al.,
a peridinioid ancestor (Skovgaard et al., 2007). The pho- 2001; Hackett et al., 2004). A single dinoflagellate cell may
totrophy may be primarily a mechanism to increase survival harbour plastids from different algal groups (Phalacroma
during dispersal of the infective spores. mitra; Nishitani et al., 2012). Several dinoflagellates of the
The richness of parasites in continental waters is rela- family Dinotrichaceae are known to possess an endosymbi-
tively low, and in general freshwater parasites are less harm- otic diatom or diatom-like alga that is separated from the di-
ful than marine ones. Cystodinedria, Cystodinium and Sty- noflagellate cytoplasm by a single unit membrane (Takano
lodinium appear to rely on photosynthesis during much of et al., 2008). Other symbionts have been reported in
their life cycle and were long believed to be strict autotrophs Amphisolenia, Amylax, Noctiluca, Podolampas (see refer-
(Cachon & Cachon, 1987; Popovský & Pfiester, 1990). The ences in Hansen, 2011), and cryptophytes in Gymnodinium
number of species of freshwaters parasites could be over- (Yamaguchi et al., 2011). This study has excluded as mu-
estimated, because numerous life stages of known species tualist symbiosis the associations where the dinoflagellate
may have been described as separate species. Crepidoo- acts as host. Numerous dinophysoid dinoflagellates contain
dinium spp. cause little damage to their hosts and may unicellular cyanobacteria which live in a hollow chamber
be ectocommensals, rather than true parasites (Lom et al., formed by a cingular list, and Ornithocercus also harbour
1993). The plastid-containing parasite Piscinoodinium be- diazotrophic heterotrophic bacteria attached to the sulcal
longs to the main clade of mutualist symbionts (Symbio- list (Farnelid et al., 2010). The same symbiont cyanobac-
dinium) (Siano et al., 2010). teria appear in a variety of dinophysoid hosts, and a sin-
The number of mutualist symbiotic species (21 species, gle dinoflagellate host may harbour mixed assemblages of
<1% total species) is low, and all species are exclusively cyanobacteria (Foster et al., 2006). The host dinoflagel-
known from warm oceans. The 15 species of Symbio- late ingests the cyanobacteria along with other prey items
dinium have a high ecological relevance in the coral (Tarangkoon et al., 2010). The population of symbiont
reefs. Symbiodinium displays a high genetic diversity, cyanobacteria is favoured by the protection, buoyancy and
which suggests a high number of undescribed species excretion products of the dinoflagellate host. However, the
(McNally et al., 1994). Dinokaryotic dinoflagellates are relationship is not mutually beneficial for a cyanobacteria
characterized by huge genomes (Spector, 1984; Lin, 2011). cell that is ingested by the host.
In contrast, Symbiodinium has a very small genome, which All basal dinoflagellates are heterotrophic, with the ex-
may be a possible adaptation to the symbiotic lifestyle ception of a noctilucoid genus (Spatulodinium; Gómez
(LaJeunesse et al., 2005). Mutualist symbionts associated et al., 2010b). For the dinokaryotic dinoflagellates, 1083
with planktonic rhizarians (Acantharia, Foraminifera (47%) are heterotrophic, and 1197 (52%) are plastid-
and Radiolaria) have been reported under the genera containing. We can expect that the number of heterotrophic
 274 F. Gómez

dinoflagellates is underestimated. The coloured dinoflagel- FOSTER, R.A., COLLIER, J.L. & CARPENTER, E.J. 2006. Reverse
lates have received more attention, especially those respon- transcription PCR amplification of cyanobacterial symbiont
sible for red-tides. The high availability of material from 16S rRNA sequences from single non-photosynthetic eukary-
otic marine planktonic host cells. Journal of Phycology 42,
the red tide species or the possibility to establish cultures 243–250.
allow detailed morphological, ultrastructural and molecu- GAINES, G. & ELBRÄCHTER, M. 1987. Heterotrophic nutrition. In:
lar phylogeny studies. In contrast, the heterotrophic species TAYLOR, F.J.R., Ed., The Biology of Dinoflagellates. Blackwell
are less visible, and usually the scarce material available Scientific Publications, Oxford, pp. 224–268.
restricts the species description. GARCÍA-CUETOS, L., MOESTRUP, Ø., HANSEN, P.J. & DAUGBJERG,
N. 2010. The toxic dinoflagellate Dinophysis acuminata har-
Consequently, our knowledge of the dinoflagellate is bors permanent chloroplasts of cryptomonad origin, not klep-
highly heterogeneous. Because of their ecological and evo- tochloroplasts. Harmful Algae 9, 25–38.
lutionary importance, dinoflagellates have a relatively well- GÓMEZ, F. 2012. A checklist and classification of living dinoflag-
developed taxonomy for certain groups such as the toxic ellates (Dinoflagellata, Alveolata). CICIMAR Oceánides 27,
species of Gonyaulacales (Alexandrium), and others (Sym- 65–140.
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012

GÓMEZ, F., LÓPEZ-GARCÍA, P. & MOREIRA, D. 2009a. Molecular

biodinium). A greater effort is needed to investigate the phylogeny of the ocelloid-bearing dinoflagellates Erythropsi-
unknown diversity, especially at greater ocean depths and dinium and Warnowia (Warnowiaceae, Dinophyceae). Jour-
the deep-ocean floor. nal of Eukaryotic Microbiology 56, 440–445.
GÓMEZ, F., LÓPEZ-GARCÍA, P., NOWACZYK, A. & MOREIRA, D.
2009b. The crustacean parasites Ellobiopsis Caullery, 1910
and Thalassomyces Niezabitowski, 1913 form a monophyletic
Acknowledgements divergent clade within the Alveolata. Systematic Parasitology
F.G. is supported by the contract JCI-2010-08492 of the 74, 65–74.
Ministerio Español de Ciencia y Tecnologı́a. GÓMEZ, F., MOREIRA, D. & LÓPEZ-GARCÍA, P. 2009c. Life cycle
and molecular phylogeny of the dinoflagellates Chytriodinium
and Dissodinium, ectoparasites of copepod eggs. European
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