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

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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
marine and freshwaters. Their adaptation to a wide range
of environments is reflected by tremendous morphologi-
cal and trophic diversity (Taylor, 1987). Like their alveo-
late relatives, apicomplexans and ciliates, the dinoflagellate
cortex has a set of flattened vesicles referred to as alveoli.
Dinoflagellates possess a ribbon-like transverse flagellum
encircling the cell and another longitudinal flagellum. For
the dinoflagellate core, the nucleus, dinokaryon, contains
large amounts of DNA and unique cytological features such
as permanently condensed chromosomes and a lack of typi-
cal eukaryotic histones (Spector, 1984; Lin, 2011). Among
the basal dinoflagellates, the syndinian nucleus is much
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
causing harmful algal blooms. Furthermore, dinoflagellates
can be either ecto- or endoparasites (Chatton, 1920; Cachon
& Cachon, 1987; Coats, 1999). As mutualistic symbionts,
dinoflagellates provide essential nutrients to most corals
and numerous other marine invertebrates, supporting coral
Correspondence to: Fernando Gómez. E-mail: fernando.gomez@
fitoplancton.com
1993; LaJeunesse, 2002).
Dinoflagellates show a high versatility in the habitat
distribution, marine or continental waters, and adaptation
to pelagic or benthic environments. They also show a high
trophic diversity (reviewed by Gaines & Elbrächter, 1987;
Stoecker, 1999; Hansen, 2011). However, no review has
ever reported the precise number of species associated
with each type of habitat, lifestyle or trophic diversity.
This analysis reviews these general trends based on data
of each dinoflagellate species. The aim of this study was to
provide a general view of the habitat distribution, lifestyle
and trophic diversity, using quantitative data of the whole
dinoflagellate group.
Materials and methods
The primary source for analysis is the checklist of living
dinoflagellates by Gómez (2012) that listed 2377 described
species. The information on each species has been labelled
according to its habitat distribution (marine or continental,
and planktonic or benthic), lifestyle (free-living, parasitic or
mutualistic symbiont), and trophic diversity (heterotrophic
and plastid-containing). The database is provided (Table
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
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268
F. Gómez
 Lifestyle, habitat and trophic diversity of dinoflagellates 269

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

habitat distribution concerns the species living in the water
column (plankton) or associated with the bottom (benthic).
This distinction is not clear-cut because the turbulence may
re-suspend the benthic species (tychoplankton), and plank-
tonic species have benthic life stages (e.g. cysts). In the case
of the parasites, they are considered planktonic or benthic
according to the habitat of their hosts, although the infecting
dinospores disperse in the water column.
The lifestyle of dinoflagellates is divided into free-living
and symbiotic species. The latter are divided into mutual-
istic symbionts (i.e. both organisms benefit), and parasites
(the dinoflagellate benefits at the expense of the host). The
distinction between parasitic and heterotrophic dinoflag-
ellate is not immediate. Parasitic dinoflagellates are con-
sidered those forms that have morphologically different
feeding and reproductive stages and that produce more
than two daughter cells after each feeding event (Gaines &
Elbrächter, 1987). The dinoflagellates are considered mu-
tualistic symbionts when the dinoflagellate is smaller than
the host as occurred in corals, various types of anemones,
jellyfish and molluscs of the reef, and in planktonic Acan-
tharia, Foraminifera and Radiolaria (Spero & Angel, 1991).
In other cases, the dinoflagellate is larger than the sym-
biont and it acts as a host (as has occurred in some
dinoflagellate–cyanobacteria consortia). This is not consid-
ered a symbiotic or parasitic relationship, and the dinoflag-
ellates are labelled as free-living heterotrophic species.
Dinoflagellates have been traditionally categorized as au-
totrophic or heterotrophic, based on the presence or absence
are labelled as ‘heterotrophic’. It is more difficult to find
a term for the species that possess plastids (auxotrophic,
autotrophic, mixotrophic, photosynthetic). Thus, the rest of
the taxa are pooled as ‘plastid-containing’ species. Many
of the original species descriptions did not specify the pres-
ence or absence of chloroplasts, or in some cases the food
contents were misinterpreted as plastids. This distinction is
subjected to the difficulties to determine the trophic char-
acter of numerous species.
Results
Trends in habitat distribution
The dinoflagellates have reached high morphological di-
versity (Fig. 1) and show higher species richness in marine
environments. From the total of 2377 described species of
dinoflagellates, 1957 species (82%) were described from
marine waters (including estuaries and brackish coastal
environments) (Figs 2–17). Most of the marine dinoflag-
ellates were free-living and marine parasites encompassed
137 species (Fig. 3). All the described dinoflagellates living
in beneficial symbiotic consortia were marine (21 species,
1%). Marine dinoflagellates are dominated by planktonic
species (1787 species, 91%), with 170 benthic species
(9%) (Fig. 16). The number of heterotrophic species in
marine environments was slightly higher (1131 species,
58%) than for plastid-containing species (Table S2, see
supplementary material, which is available on the Sup-
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
the basal dinoflagellates have been described from ma-
rine waters. Among the Dinokaryota, the order Dino-
physales is exclusively composed of marine species,
and Prorocentrales and Gonyaulacales were highly dom-
inated by marine species (Table S1, see supplemen-
tary material, which is available on the Supplementary
tab of the article’s Taylor & Francis Online page at
http://dx.doi/10.1080/14772000.2012.721021).
A total of 420 species have been described from
continental waters (17% of 2377 species) (Fig. 4). A few
freshwater species were benthic (30 species, 7%), mainly
composed of a group of insufficiently known taxa represent-
ing the genera, Cystodinium, Stylodinium and Tetradinium.
In contrast to the marine species, the continental species
were highly dominated by plastid-containing species (88%)
(Fig. 8). The few heterotrophic species (48 species, 11%)
were little-known species of the genera Gymnodinium,
Gyrodinium, Katodinium or Stylodinium. The percentage
of parasitic species in continental waters (27 species,
6%) was slightly lower than in marine waters (Fig. 12).
Several genera of continental parasites contained plastids
 Lifestyle, habitat and trophic diversity of dinoflagellates
(Cystodinium, Crepidoodinium) and others were devoid of
plastids (Cystodinedria, Oodinioides and Stylodinium).
Concerning the distribution of dinoflagellates in the
water column, most were planktonic (2177, 91%) (Fig. 5).
These planktonic species were preferentially marine (1787,
91%), and about one half contained plastids (Fig. 9). A total
of 127 (5%) species were parasites. There were 200 species
described from benthic environments (8% of total), mainly
algal epiphytes or sand-dwelling species (episammic).
Most of the benthic species were marine (170 species, 85%)
and plastid-containing (133 species, 66%) (Table S2, see
supplementary material, which is available on the Supple-
mentary tab of the article’s Taylor & Francis Online page
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012
at http://dx.doi/10.1080/14772000.2012.721021). Benthic
species have not been described among basal dinoflagel-
lates, with the exception of Hematodinium, which para-
sitizes benthic crustaceans. Among the dinokaryonts, the
order Gonyaulacales showed a high proportion of benthic
species due to the epiphytic genera, Coolia, Gambierdiscus,
Ostreopsis and the sand-dwelling Thecadinium. The per-
centage of benthic parasitic species (37 species, 18%) was
higher than for the planktonic species. The benthic parasites
belonged to the heterotrophic genera, Haplozoon and Stylo-
dinium, and the plastid-containing Cystodinium. Among the
beneficial symbiotic species, Symbiodinium spp. and Am-
phidinium belauense are associated with benthic organisms
(Table S1, see supplementary material, which is available on
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-
containing species (Figs 3, 7). A total of 164 dinoflagellates
species (6.8%) were parasites. About one half of the para-
sites were basal dinoflagellates (77 species), and 87 species
were dinokaryotic parasites. Most of the parasites were het-
erotrophs, with the exceptions of 34 species that contained
plastids. The main representatives of the plastid-containing
parasites were Blastodinium, a parasite of marine cope-
pods, Crepidoodinium and Piscinoodinium, parasites of
freshwater fishes, and the insufficiently known species of
Cystodinium, a parasite of freshwater algae (Table S1,
see supplementary material, which is available on the Sup-
plementary tab of the article’s Taylor & Francis Online page
at http://dx.doi/10.1080/14772000.2012.721021).
There were 21 species of dinoflagellates living in
a mutually endosymbiotic association. The genus Sym-
biodinium with 15 species and one species of Pelago-
dinium (family Symbiodinium) constituted the main
clade of mutualist symbionts (Table S1, see supplemen-
tary material, which is available on the Supplementary
tab of the article’s Taylor & Francis Online page at
http://dx.doi/10.1080/14772000.2012.721021).
271
Trends in trophism
The heterotrophic species constituted 49% of the to-
tal species (1179 species) (Fig. 2). They slightly dom-
inate in marine waters, while the proportion was low
in continental waters with only 48 heterotrophic species.
Most of the parasites were heterotrophic (130/164 species)
(Fig. 6), and about 30% of the benthic species were het-
erotrophic (67/200 species) (Fig. 14). All the basal di-
noflagellates were heterotrophs, with the exception of
a life stage of Spatulodinium, known as Gymnodinium
lebouriae that contained plastids (Table S1, see supple-
mentary material, which is available on the Supplemen-
tary tab of the article’s Taylor & Francis Online page at
http://dx.doi/10.1080/14772000.2012.721021). Among the
2280 dinokaryotic dinoflagellates, 1083 species (48%) are
heterotrophs. None of the classical major orders (Peri-
diniales, Gymnodiniales, Prorocentrales, Dinophysales,
Gonyaulacales) is exclusively constituted of heterotrophic
species. Most of Dinophysales were heterotrophic, with the
exception of some Dinophysis and a few Phalacroma. Sev-
eral families of Peridiniales sensu lato were exclusively
heterotrophic species such as Amphidiniopsidaceae, Het-
erodiniaceae, Podolampadaceae and Protoperidiniaceae. In
contrast, the orders Brachidiniales and Prorocentrales were
exclusively composed of plastid-containing species, as well
as the families Dinotrichaceae, Glenodiniaceae, Heterocap-
saceae, Peridiniaceae sensu stricto and Symbiodiniaceae
(Table S1, see supplementary material, which is available on
the Supplementary tab of the article’s Taylor & Francis On-
line page at http://dx.doi/10.1080/14772000.2012.721021).
Discussion
Trends in the habitat distribution
Most major microbial lineages originated in ancient oceans
(e.g. Cavalier-Smith, 2006). Dinoflagellates show a higher
species richness in marine environments (four of each five
species). Bourrelly (1970) and Taylor (1987, p. 409) re-
ported that approximately only 220 species inhabit fresh-
water environments. This study listed 420 species living
in continental waters. The proportion of marine species
could be higher because: (1) for species descriptions, the
continental waters have been historically more investigated
than the oceans; (2) it could be an excess of species de-
scribed for several freshwater genera such as Cystodinium,
Hemidinium or Tetradinium because they may correspond
to life stages of other known species (i.e. Baumeister, 1957;
Skvortzov, 1968), as well as many insufficiently known
freshwater species of Amphidinium and Gymnodinium;
and (3) environmental sequencing of the deep open ocean
or deep sediments revealed numerous novel heterotrophic
clades dinoflagellates, that have not been morphologically
characterized (López-Garcı́a et al., 2001, 2007). They are
 272 F. Gómez
often in smaller size fractions (<5 µm) that are difficult to
examine and differentiate by classical methods.
Several species of dinoflagellates are adapted to high
fluctuations of salinity (e.g. Oxyrrhis). However, no species
is able to proliferate in both oligohaline and marine waters.
Logares et al. (2007) concluded that marine and freshwa-
ter dinoflagellates are usually not closely related, several
freshwater species cluster into monophyletic groups, only
a small fraction of the marine lineages seem to have colo-
nized freshwaters, and most marine–freshwater transitions
do not seem to have occurred recently.
As an example, the type species of the specious genus
Gymnodinium is a photosynthetic freshwater species. The
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012
support for the divergence between marine and continen-
tal species of Gymnodinium increases in more complete
phylogenetic trees, including the families Chytriodiniaceae
and Warnowiaceae (Gómez et al., 2009a, 2009c). Genera
such as Amphidiniopsis, Gyrodinium or Prorocentrum con-
tain both marine and freshwater species. However, in some
cases, such as Gyrodinium, the addition of more species se-
quences into the molecular phylogenies could support the
generic separation of marine and freshwater species. The
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
speciation, while the freshwater Ceratium is restricted to a
few species.
The present study reveals that continental waters showed
a high percentage of plastid-containing species (88%).
Dinoflagellates have a lower photosynthetic efficiency
than other protist groups (Morse et al., 1995; Tang, 1996).
This may constitute a disadvantage to proliferate in the
oligotrophic open ocean. In contrast, the higher nutrient
concentrations in the continental waters may favour
the development of plastid-containing dinoflagellates.
Dinoflagellates possess the most diverse array of plastids
of any eukaryotic lineage (Saldarriaga et al., 2001; Hackett
et al., 2004). However, the pigment composition of the
continental species is less diverse than for the marine ones.
Common freshwater genera such as Peridinium or Gymno-
dinium contain the most typical chloroplast of dinoflagel-
lates, which is bounded by three membranes and possess
chlorophylls a and c2 as well as peridinin as a major acces-
sory pigment. A few freshwater dinoflagellates, as well as
marine species, have a blue pigment, phycobilin, obtained
from a cryptophyte endosymbiont (Yamaguchi et al., 2011).
Most of the dinoflagellates are planktonic in marine
and continental ecosystems. Taylor et al. (2008, p. 408)
estimated 160 marine benthic species, and they reported
that only one explicitly freshwater benthic species has been
described. From the 200 species of benthic dinoflagellates,
85% inhabit marine and 15% continental waters (Figs 2–17,
Table S2, see supplementary material, which is available on
the Supplementary tab of the article’s Taylor & Francis On-
line page at http://dx.doi/10.1080/14772000.2012.721021).
Little-known freshwater genera, with an apparent excess
of species (Cystodinium, Stylodinium and Tetradinium),
may reduce the proportion of benthic species in continental
waters. Many of these species are parasites of benthic
hosts. They are not highly flattened as typical in benthic
dinoflagellates. Only three species of Prorocentrum (=
?Haplodinium antjoliense) and Amphidiniopsis sibbaldii
showed flattened morphologies in freshwater environments.
Historically, the benthic dinoflagellates have received
less attention than the pelagic species. Beyond a few pi-
oneer studies (Herdman, 1924; Balech, 1956), the ben-
thic species have been undersampled for decades. A high
number of marine benthic species have been described in
the last 20 years, especially species associated with the
ciguatera in tropical waters (Coolia, Gambierdiscus, Os-
treopsis, Prorocentrum). The sampling coverage of benthic
species is nearly restricted to shallow waters as epiphytes of
macrophytes, coral reefs or sandy beaches. Environmental
sequencing libraries revealed that there may be consider-
ably high diversity of undescribed heterotrophic or parasitic
species yet to be described in the deep ocean floor (Moreira
& López-Garcı́a, 2003).
Trends in lifestyle
Most of the dinoflagellates were free-living species (92%
of 2377). In contrast, the closest relatives to the dinoflag-
ellates, apicomplexans and perkinsids, and nearly all the
basal dinoflagellates are parasites (Zhang et al., 2011).
Cachon & Cachon (1987) listed 66 parasitic dinoflag-
ellates, and Drebes (1984) estimated about 140 species.
Taylor et al. (2008) estimated parasites were 5% of the total
species. The present study reported 164 species of para-
sites (7% of the total 2377 species). About one half of the
total species (77 species) belong to the non-dinokaryotic
basal dinoflagellates (ellobiopsids, Duboscquodinida, Syn-
diniales). In the molecular phylogenies, a few free-living
species branched among the basal dinoflagellates (Oxyrrhis
and Noctilucales) (Saldarriaga et al., 2003; Gómez et al.,
2010b). Oxyrrhis is a free-living species that only prolif-
erates in brackish environments, often associated with the
unialgal blooms (Dunaliella). The morphology of Oxyrrhis
resembles the dispersive spores of Syndiniales (Chatton,
1920; Skovgaard et al., 2005).
To date, environmental sequences of Duboscquodinida
(Marine Alveolate Group I) and Syndiniales (Marine Alve-
olate Group II) have been retrieved exclusively from marine
environments (Guillou et al., 2008). Syndiniales are geneti-
cally more diverse than Duboscquodinida, and the diversity
in the deep-ocean and deep floor is greatly underestimated,
because there are more clades than known species (Guillou
et al., 2008). All the ellobiopsids were described from
marine waters (Gómez et al., 2009b), although infections
by ellobiopsid parasites have been reported in freshwater
crustaceans (Bridgeman et al., 2000; Manca et al., 2004).
 Lifestyle, habitat and trophic diversity of dinoflagellates
The basal dinoflagellates are considerably dominated by
parasites, while the proportion of parasites is low (3%)
among the typical dinoflagellates. The parasitism in di-
nokaryotes is restricted to 87 species which were often
dispersed among free-living species. Haplozoon is a para-
site with a basal position in the dinokaryotic core (Cachon
& Cachon, 1987). However, the other clades of parasitic
dinoflagellates (Chytriodiniaceae, Oodiniaceae, Piscinood-
inium) emerge among free-living forms, and suggest that
parasitism is a recent acquisition. So far, the parasitic basal
dinoflagellates do not contain plastids, while about 40%
of the dinokaryotic parasites contain plastids. Nearly all
the species of Blastodinium contain plastids, although the
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photosynthesis partially covers the cell requirements and
the rest being ensured by the assimilation of host diges-
tive substances (Pasternak et al., 1984). The parasites of
the family Chytriodiniaceae (Chytriodinium, Dissodinium)
emerged among clades of photosynthetic species of Gymno-
dinium. The parasite of copepod eggs, Dissodinium pseu-
dolunula, possesses plastids, while its closer relatives are
heterotrophic species (Gómez et al., 2009c). This suggests
a recent loss of the plastids in Chytriodiniaceae, more than
a recent acquisition in D. pseudolunula. The presence of
plastids seems to be a reminiscent of its photosynthetic
ancestor in Dissodinium and Blastodinium, the latter with
a peridinioid ancestor (Skovgaard et al., 2007). The pho-
totrophy may be primarily a mechanism to increase survival
during dispersal of the infective spores.
The richness of parasites in continental waters is rela-
tively low, and in general freshwater parasites are less harm-
ful than marine ones. Cystodinedria, Cystodinium and Sty-
lodinium appear to rely on photosynthesis during much of
their life cycle and were long believed to be strict autotrophs
(Cachon & Cachon, 1987; Popovský & Pfiester, 1990). The
number of species of freshwaters parasites could be over-
estimated, because numerous life stages of known species
may have been described as separate species. Crepidoo-
dinium spp. cause little damage to their hosts and may
be ectocommensals, rather than true parasites (Lom et al.,
1993). The plastid-containing parasite Piscinoodinium be-
longs to the main clade of mutualist symbionts (Symbio-
dinium) (Siano et al., 2010).
The number of mutualist symbiotic species (21 species,
<1% total species) is low, and all species are exclusively
known from warm oceans. The 15 species of Symbio-
dinium have a high ecological relevance in the coral
reefs. Symbiodinium displays a high genetic diversity,
which suggests a high number of undescribed species
(McNally et al., 1994). Dinokaryotic dinoflagellates are
characterized by huge genomes (Spector, 1984; Lin, 2011).
In contrast, Symbiodinium has a very small genome, which
may be a possible adaptation to the symbiotic lifestyle
(LaJeunesse et al., 2005). Mutualist symbionts associated
with planktonic rhizarians (Acantharia, Foraminifera
and Radiolaria) have been reported under the genera
273
Amphidinium, Aureodinium, Gloeodinium, Gymnodinium,
Gyrodinium, Prorocentrum, Pyrocystis and Scrippsiella
(Spero & Angel, 1991). However, the precise identification
of many of these species and its interpretation as mutualist
symbionts is doubtful. The molecular phylogenies support
the polyphyletic origin of dinoflagellate-invertebrate
symbiosis (McNally et al., 1994). Mutualist symbionts
are separated into at least three clades (Table S1, see
supplementary material, which is available on the Sup-
plementary tab of the article’s Taylor & Francis Online
page at http://dx.doi/10.1080/14772000.2012.721021). In
addition to Symbiodinium, the family Symbiodiniaceae,
contain numerous free-living species, and Piscinoodinium,
a plastid-containing species that is parasitic on freshwater
fishes, and the symbionts of planktonic foraminifera
Pelagodinium (formerly Gymnodinium) (Siano et al.,
2010). The family Endodiniaceae, including Endodinium,
have reported under the genera Amphidinium, Gloeo-
dinium, Scrippsiella and Zooxanthella (Spero & Angel,
1991). A third clade is composed of a single species,
Amphidinium belauense, living in a flatworm, closely re-
lated to free-living photosynthetic species of Amphidinium
sensu stricto (McNally et al., 1994).
Dinoflagellates show a high proclivity for endosymbio-
sis, which is largely reported for plastids (Saldarriaga et al.,
2001; Hackett et al., 2004). A single dinoflagellate cell may
harbour plastids from different algal groups (Phalacroma
mitra; Nishitani et al., 2012). Several dinoflagellates of the
family Dinotrichaceae are known to possess an endosymbi-
otic diatom or diatom-like alga that is separated from the di-
noflagellate cytoplasm by a single unit membrane (Takano
et al., 2008). Other symbionts have been reported in
Amphisolenia, Amylax, Noctiluca, Podolampas (see refer-
ences in Hansen, 2011), and cryptophytes in Gymnodinium
(Yamaguchi et al., 2011). This study has excluded as mu-
tualist symbiosis the associations where the dinoflagellate
acts as host. Numerous dinophysoid dinoflagellates contain
unicellular cyanobacteria which live in a hollow chamber
formed by a cingular list, and Ornithocercus also harbour
diazotrophic heterotrophic bacteria attached to the sulcal
list (Farnelid et al., 2010). The same symbiont cyanobac-
teria appear in a variety of dinophysoid hosts, and a sin-
gle dinoflagellate host may harbour mixed assemblages of
cyanobacteria (Foster et al., 2006). The host dinoflagel-
late ingests the cyanobacteria along with other prey items
(Tarangkoon et al., 2010). The population of symbiont
cyanobacteria is favoured by the protection, buoyancy and
excretion products of the dinoflagellate host. However, the
relationship is not mutually beneficial for a cyanobacteria
cell that is ingested by the host.
All basal dinoflagellates are heterotrophic, with the ex-
ception of a noctilucoid genus (Spatulodinium; Gómez
et al., 2010b). For the dinokaryotic dinoflagellates, 1083
(47%) are heterotrophic, and 1197 (52%) are plastid-
containing. We can expect that the number of heterotrophic
 274 F. Gómez
dinoflagellates is underestimated. The coloured dinoflagel-
lates have received more attention, especially those respon-
sible for red-tides. The high availability of material from
the red tide species or the possibility to establish cultures
allow detailed morphological, ultrastructural and molecu-
lar phylogeny studies. In contrast, the heterotrophic species
are less visible, and usually the scarce material available
restricts the species description.
Consequently, our knowledge of the dinoflagellate is
highly heterogeneous. Because of their ecological and evo-
lutionary importance, dinoflagellates have a relatively well-
developed taxonomy for certain groups such as the toxic
species of Gonyaulacales (Alexandrium), and others (Sym-
Downloaded by [University of Valencia], [Fernando Gomez] at 01:57 20 September 2012
biodinium). A greater effort is needed to investigate the
unknown diversity, especially at greater ocean depths and
the deep-ocean floor.
Acknowledgements
F.G. is supported by the contract JCI-2010-08492 of the
Ministerio Español de Ciencia y Tecnologı́a.
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