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

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
Instituto Cavanilles de Biodiversidad y Biología 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
The dinoflagellates are an important group of protists in
marine and freshwaters. Their adaptation to a wide range
of environments is reflected by tremendous morphological
and trophic diversity (Taylor, 1987). Like their alveolate
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 typical
eukaryotic histones (Spector, 1984; Lin, 2011). Among
the basal dinoflagellates, the syndinian nucleus is much
closer to the eukaryotic type. Dinoflagellates are both primary
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
reefs, one of the most diverse ecosystems on Earth (Trench,
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

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 continental
waters. However, the distinction for marine or continental
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 estuaries
and brackish coastal environments (Kryptoperidinium,
Oxyrrhis, Pfiesteria) are labelled as marine species. Other
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 planktonic
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 mutualistic
symbionts (i.e. both organisms benefit), and parasites
(the dinoflagellate benefits at the expense of the host). The
distinction between parasitic and heterotrophic dinoflagellate
is not immediate. Parasitic dinoflagellates are considered
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 mutualistic
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 Acantharia,
Foraminifera and Radiolaria (Spero & Angel, 1991).
In other cases, the dinoflagellate is larger than the symbiont
and it acts as a host (as has occurred in some
dinoflagellate–cyanobacteria consortia). This is not considered
a symbiotic or parasitic relationship, and the dinoflagellates
are labelled as free-living heterotrophic species.
Dinoflagellates have been traditionally categorized as autotrophic
or heterotrophic, based on the presence or absence
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 dinoflagellates,
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. Dinophysis,
García-Cuetos et al., 2010; Pfiesteria, Feinstein
et al., 2002). The species devoid of plastids or pigments
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 presence
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 character
of numerous species.
Results
Trends in habitat distribution
The dinoflagellates have reached high morphological diversity
(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 dinoflagellates
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 Supplementary
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
PLASTID-
CONTAINING
HETERO-
TROPHIC
FREE-
LIVING
PARASITE
SYMBIOSIS
MARINE
CONTINENTAL
PLANKTON
BENTHIC
6
SYM
PAR
FREE-
LIVING
PARASITE
FREE-
LIVING
FREE
7
HETERO-
TROPHIC
PLASTID-
CONTAINING
FREE-LIVING
HET
PARASITE
8
HETERO-
TROPHIC
MARINE
CHL
PLASTID-
CONTAINING
HET
CONTINENTAL
9
HETERO-
TROPHIC
PLANKTON
PLASTID-
CONTAINING
CHL
HET
BENTHIC
10
plastid-
CONTINENTAL
MARINE
heterotrophic
CONTINENTAL
MARINE
11
MARINE
CONTINENTAL
MARINE
PARASITE
12
FREE-
LIVING
PARASITE
SYM
FREE-
LIVING
CONTINENTAL
PAR
13
FREE-
LIVING
PARASITE
FRE
BENTHIC
FREE-LIVING
MARINE
PLANKTON
14
plastid-
BENTHIC
PLANKTON
heterotrophic
BENTHIC
PLANKTON
15
PLANKTON
BENTHIC
PLK
PARASITE
16
BENTHIC
BEN
PLANKTON
PLANKTON
CONTINENTAL
17
CONTINENTAL
MAR
MARINE
CON
BENTHIC
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 plastidcontaining
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 marine
waters. Among the Dinokaryota, the order Dinophysales
is exclusively composed of marine species,
and Prorocentrales and Gonyaulacales were highly dominated
by marine species (Table S1, see supplementary
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 representing
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 271
(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 Supplementary
tab of the article’s Taylor & Francis Online page
at http://dx.doi/10.1080/14772000.2012.721021). Benthic
species have not been described among basal dinoflagellates,
with the exception of Hematodinium, which parasitizes
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 percentage
of benthic parasitic species (37 species, 18%) was
higher than for the planktonic species. The benthic parasites
belonged to the heterotrophic genera, Haplozoon and Stylodinium,
and the plastid-containing Cystodinium. Among the
beneficial symbiotic species, Symbiodinium spp. and Amphidinium
belauense are associated with benthic organisms
(Table S1, see supplementary 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).
Trends in the lifestyle
The dinoflagellates are dominated by free-living species
(2192 species, 92%) of which 1143 or 52% are plastidcontaining
species (Figs 3, 7). A total of 164 dinoflagellates
species (6.8%) were parasites. About one half of the parasites
were basal dinoflagellates (77 species), and 87 species
were dinokaryotic parasites. Most of the parasites were heterotrophs,
with the exceptions of 34 species that contained
plastids. The main representatives of the plastid-containing
parasites were Blastodinium, a parasite of marine copepods,
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 Supplementary
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 Symbiodinium
with 15 species and one species of Pelagodinium
(family Symbiodinium) constituted the main
clade of mutualist symbionts (Table S1, see supplementary
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).
Trends in trophism
The heterotrophic species constituted 49% of the total
species (1179 species) (Fig. 2). They slightly dominate
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 heterotrophic
(67/200 species) (Fig. 14). All the basal dinoflagellates
were heterotrophs, with the exception of
a life stage of Spatulodinium, known as Gymnodinium
lebouriae that contained plastids (Table S1, see supplementary
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). Among the
2280 dinokaryotic dinoflagellates, 1083 species (48%) are
heterotrophs. None of the classical major orders (Peridiniales,
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.Several
families of Peridiniales sensu lato were exclusively
heterotrophic species such as Amphidiniopsidaceae, Heterodiniaceae,
Podolampadaceae and Protoperidiniaceae. In
contrast, the orders Brachidiniales and Prorocentrales were
exclusively composed of plastid-containing species, as well
as the families Dinotrichaceae, Glenodiniaceae, Heterocapsaceae,
Peridiniaceae sensu stricto and Symbiodiniaceae
(Table S1, see supplementary 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).
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) reported
that approximately only 220 species inhabit freshwater
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 described
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-García et al., 2001, 2007). They are

272 F. Gómez
often in smaller size fractions (

Lifestyle, habitat and trophic diversity of dinoflagellates 273
The basal dinoflagellates are considerably dominated by
parasites, while the proportion of parasites is low (3%)
among the typical dinoflagellates. The parasitism in dinokaryotes
is restricted to 87 species which were often
dispersed among free-living species. Haplozoon is a parasite
with a basal position in the dinokaryotic core (Cachon
& Cachon, 1987). However, the other clades of parasitic
dinoflagellates (Chytriodiniaceae, Oodiniaceae, Piscinoodinium)
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
photosynthesis partially covers the cell requirements and
the rest being ensured by the assimilation of host digestive
substances (Pasternak et al., 1984). The parasites of
the family Chytriodiniaceae (Chytriodinium, Dissodinium)
emerged among clades of photosynthetic species of Gymnodinium.
The parasite of copepod eggs, Dissodinium pseudolunula,
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 phototrophy
may be primarily a mechanism to increase survival
during dispersal of the infective spores.
The richness of parasites in continental waters is relatively
low, and in general freshwater parasites are less harmful
than marine ones. Cystodinedria, Cystodinium and Stylodinium
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 overestimated,
because numerous life stages of known species
may have been described as separate species. Crepidoodinium
spp. cause little damage to their hosts and may
be ectocommensals, rather than true parasites (Lom et al.,
1993). The plastid-containing parasite Piscinoodinium belongs
to the main clade of mutualist symbionts (Symbiodinium)
(Siano et al., 2010).
The number of mutualist symbiotic species (21 species,

274 F. Gómez
dinoflagellates is underestimated. The coloured dinoflagellates
have received more attention, especially those responsible
for red-tides. The high availability of material from
the red tide species or the possibility to establish cultures
allow detailed morphological, ultrastructural and molecular
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 evolutionary
importance, dinoflagellates have a relatively welldeveloped
taxonomy for certain groups such as the toxic
species of Gonyaulacales (Alexandrium), and others (Symbiodinium).
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 Tecnología.
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Associate Editor: Elliot Shubert