Systematics and Biodiversity (2012), 10(3): 267275

Perspective A quantitative review of the lifestyle, habitat and trophic diversity of dinoagellates (Dinoagellata, Alveolata)

FERNANDO GOMEZ
Instituto Cavanilles de Biodiversidad y Biolog a 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 dinoagellates (Dinophyceae). Most of the dinoagellates inhabit marine waters, whereas 17% of the total species have colonized continental waters. Dinoagellates 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 dinoagellates (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 dinoagellates 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 benecial 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 dinoagellates are an important group of protists in marine and freshwaters. Their adaptation to a wide range of environments is reected by tremendous morphological and trophic diversity (Taylor, 1987). Like their alveolate relatives, apicomplexans and ciliates, the dinoagellate cortex has a set of attened vesicles referred to as alveoli. Dinoagellates possess a ribbon-like transverse agellum encircling the cell and another longitudinal agellum. For the dinoagellate 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 dinoagellates, the syndinian nucleus is much closer to the eukaryotic type. Dinoagellates 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, dinoagellates can be either ecto- or endoparasites (Chatton, 1920; Cachon & Cachon, 1987; Coats, 1999). As mutualistic symbionts, dinoagellates provide essential nutrients to most corals and numerous other marine invertebrates, supporting coral
Correspondence to: Fernando G omez. E-mail: fernando.gomez@ toplancton.com
ISSN 1477-2000 print / 1478-0933 online C 2012 The Natural History Museum http://dx.doi.org/10.1080/14772000.2012.721021

reefs, one of the most diverse ecosystems on Earth (Trench, 1993; LaJeunesse, 2002). Dinoagellates 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 & Elbr achter, 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 dinoagellate 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 dinoagellate group.

Materials and methods

The primary source for analysis is the checklist of living dinoagellates by G omez (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

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Lifestyle, habitat and trophic diversity of dinoagellates Supplementary tab of the articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021). However, information on a precise species should be veried in the specic literature. There are no examples of dinoagellate species which are able to proliferate in both marine and oligohaline continental waters. However, the distinction for marine or continental species may be difcult for some species described from estuarine or coastal brackish waters subjected to strong uctuations in salinity. At these locations, continental and marine species may co-exist. Species described from estuaries and brackish coastal environments (Kryptoperidinium, Oxyrrhis, Pesteria) 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 dinoagellates is divided into free-living and symbiotic species. The latter are divided into mutualistic symbionts (i.e. both organisms benet), and parasites (the dinoagellate benets at the expense of the host). The distinction between parasitic and heterotrophic dinoagellate is not immediate. Parasitic dinoagellates 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 & Elbr achter, 1987). The dinoagellates are considered mutualistic symbionts when the dinoagellate is smaller than the host as occurred in corals, various types of anemones, jellysh and molluscs of the reef, and in planktonic Acantharia, Foraminifera and Radiolaria (Spero & Angel, 1991). In other cases, the dinoagellate is larger than the symbiont and it acts as a host (as has occurred in some dinoagellatecyanobacteria consortia). This is not considered a symbiotic or parasitic relationship, and the dinoagellates are labelled as free-living heterotrophic species. Dinoagellates have been traditionally categorized as autotrophic or heterotrophic, based on the presence or absence

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of chlorophyll and plastids. It is difcult 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 dinoagellates have food vacuoles and feed on other protists (Stoecker, 1999; Jeong et al., 2005; Hansen, 2011). For some dinoagellates, 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, Garc a-Cuetos et al., 2010; Pesteria, Feinstein et al., 2002). The species devoid of plastids or pigments are labelled as heterotrophic. It is more difcult to nd 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 difculties to determine the trophic character of numerous species.

Results
Trends in habitat distribution
The dinoagellates have reached high morphological diversity (Fig. 1) and show higher species richness in marine environments. From the total of 2377 described species of dinoagellates, 1957 species (82%) were described from marine waters (including estuaries and brackish coastal environments) (Figs 217). Most of the marine dinoagellates were free-living and marine parasites encompassed 137 species (Fig. 3). All the described dinoagellates living in benecial symbiotic consortia were marine (21 species, 1%). Marine dinoagellates 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 articles Taylor & Francis Online

Fig. 1. Diversity of major lineages of dinoagellates: 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. Roscofa; 75. Lessardia; 76. Heterodinium; 77. Corythodinium; 78. Gyrodinium; 79. Hemidinium; 80. Glenodinium; 81. Pesteria; 82. Scrippsiella; 83. Oodinium.

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Figs 217. Pie charts of the percent of dinoagellates (n = 2377 species) according to the trophic classication (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 dinoagellates 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 articles 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 insufciently 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

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Lifestyle, habitat and trophic diversity of dinoagellates (Cystodinium, Crepidoodinium) and others were devoid of plastids (Cystodinedria, Oodinioides and Stylodinium). Concerning the distribution of dinoagellates 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 articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021). Benthic species have not been described among basal dinoagellates, 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 benecial 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 articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021).

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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 dinoagellates 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 articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021). Among the 2280 dinokaryotic dinoagellates, 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 articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021).

Trends in the lifestyle

The dinoagellates are dominated by free-living species (2192 species, 92%) of which 1143 or 52% are plastidcontaining species (Figs 3, 7). A total of 164 dinoagellates species (6.8%) were parasites. About one half of the parasites were basal dinoagellates (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 shes, and the insufciently known species of Cystodinium, a parasite of freshwater algae (Table S1, see supplementary material, which is available on the Supplementary tab of the articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021). There were 21 species of dinoagellates 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 articles 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). Dinoagellates show a higher species richness in marine environments (four of each ve 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 insufciently known freshwater species of Amphidinium and Gymnodinium; and (3) environmental sequencing of the deep open ocean or deep sediments revealed numerous novel heterotrophic clades dinoagellates, that have not been morphologically characterized (L opez-Garc a et al., 2001, 2007). They are

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F. G omez 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 attened as typical in benthic dinoagellates. Only three species of Prorocentrum (= ?Haplodinium antjoliense) and Amphidiniopsis sibbaldii showed attened morphologies in freshwater environments. Historically, the benthic dinoagellates have received less attention than the pelagic species. Beyond a few pioneer studies (Herdman, 1924; Balech, 1956), the benthic 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, Ostreopsis, 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 considerably high diversity of undescribed heterotrophic or parasitic species yet to be described in the deep ocean oor (Moreira & L opez-Garc a, 2003).

often in smaller size fractions (<5 m) that are difcult to examine and differentiate by classical methods. Several species of dinoagellates are adapted to high uctuations 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 freshwater dinoagellates are usually not closely related, several freshwater species cluster into monophyletic groups, only a small fraction of the marine lineages seem to have colonized freshwaters, and most marinefreshwater 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 support for the divergence between marine and continental species of Gymnodinium increases in more complete phylogenetic trees, including the families Chytriodiniaceae and Warnowiaceae (G omez et al., 2009a, 2009c). Genera such as Amphidiniopsis, Gyrodinium or Prorocentrum contain both marine and freshwater species. However, in some cases, such as Gyrodinium, the addition of more species sequences 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 (G omez 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%). Dinoagellates have a lower photosynthetic efciency 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 dinoagellates. Dinoagellates 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 Gymnodinium contain the most typical chloroplast of dinoagellates, which is bounded by three membranes and possess chlorophylls a and c2 as well as peridinin as a major accessory pigment. A few freshwater dinoagellates, as well as marine species, have a blue pigment, phycobilin, obtained from a cryptophyte endosymbiont (Yamaguchi et al., 2011). Most of the dinoagellates 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 dinoagellates, 85% inhabit marine and 15% continental waters (Figs 217, Table S2, see supplementary material, which is available on the Supplementary tab of the articles Taylor & Francis Online page at http://dx.doi/10.1080/14772000.2012.721021).

Trends in lifestyle
Most of the dinoagellates were free-living species (92% of 2377). In contrast, the closest relatives to the dinoagellates, apicomplexans and perkinsids, and nearly all the basal dinoagellates are parasites (Zhang et al., 2011). Cachon & Cachon (1987) listed 66 parasitic dinoagellates, 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 parasites (7% of the total 2377 species). About one half of the total species (77 species) belong to the non-dinokaryotic basal dinoagellates (ellobiopsids, Duboscquodinida, Syndiniales). In the molecular phylogenies, a few free-living species branched among the basal dinoagellates (Oxyrrhis and Noctilucales) (Saldarriaga et al., 2003; G omez et al., 2010b). Oxyrrhis is a free-living species that only proliferates 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 Alveolate Group II) have been retrieved exclusively from marine environments (Guillou et al., 2008). Syndiniales are genetically more diverse than Duboscquodinida, and the diversity in the deep-ocean and deep oor is greatly underestimated, because there are more clades than known species (Guillou et al., 2008). All the ellobiopsids were described from marine waters (G omez 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 dinoagellates The basal dinoagellates are considerably dominated by parasites, while the proportion of parasites is low (3%) among the typical dinoagellates. 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 dinoagellates (Chytriodiniaceae, Oodiniaceae, Piscinoodinium) emerge among free-living forms, and suggest that parasitism is a recent acquisition. So far, the parasitic basal dinoagellates 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 (G omez 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; Popovsk y & Pester, 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, <1% total species) is low, and all species are exclusively known from warm oceans. The 15 species of Symbiodinium 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 dinoagellates 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

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Amphidinium, Aureodinium, Gloeodinium, Gymnodinium, Gyrodinium, Prorocentrum, Pyrocystis and Scrippsiella (Spero & Angel, 1991). However, the precise identication of many of these species and its interpretation as mutualist symbionts is doubtful. The molecular phylogenies support the polyphyletic origin of dinoagellate-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 Supplementary tab of the articles 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 shes, and the symbionts of planktonic foraminifera Pelagodinium (formerly Gymnodinium) (Siano et al., 2010). The family Endodiniaceae, including Endodinium, have reported under the genera Amphidinium, Gloeodinium, Scrippsiella and Zooxanthella (Spero & Angel, 1991). A third clade is composed of a single species, Amphidinium belauense, living in a atworm, closely related to free-living photosynthetic species of Amphidinium sensu stricto (McNally et al., 1994). Dinoagellates show a high proclivity for endosymbiosis, which is largely reported for plastids (Saldarriaga et al., 2001; Hackett et al., 2004). A single dinoagellate cell may harbour plastids from different algal groups (Phalacroma mitra; Nishitani et al., 2012). Several dinoagellates of the family Dinotrichaceae are known to possess an endosymbiotic diatom or diatom-like alga that is separated from the dinoagellate cytoplasm by a single unit membrane (Takano et al., 2008). Other symbionts have been reported in Amphisolenia, Amylax, Noctiluca, Podolampas (see references in Hansen, 2011), and cryptophytes in Gymnodinium (Yamaguchi et al., 2011). This study has excluded as mutualist symbiosis the associations where the dinoagellate acts as host. Numerous dinophysoid dinoagellates 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 cyanobacteria appear in a variety of dinophysoid hosts, and a single dinoagellate host may harbour mixed assemblages of cyanobacteria (Foster et al., 2006). The host dinoagellate 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 dinoagellate host. However, the relationship is not mutually benecial for a cyanobacteria cell that is ingested by the host. All basal dinoagellates are heterotrophic, with the exception of a noctilucoid genus (Spatulodinium; G omez et al., 2010b). For the dinokaryotic dinoagellates, 1083 (47%) are heterotrophic, and 1197 (52%) are plastidcontaining. We can expect that the number of heterotrophic

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FOSTER, R.A., COLLIER, J.L. & CARPENTER, E.J. 2006. Reverse transcription PCR amplication of cyanobacterial symbiont 16S rRNA sequences from single non-photosynthetic eukaryotic marine planktonic host cells. Journal of Phycology 42, 243250. , M. 1987. Heterotrophic nutrition. In: GAINES, G. & ELBRACHTER TAYLOR, F.J.R., Ed., The Biology of Dinoagellates. Blackwell Scientic Publications, Oxford, pp. 224268. IA-CUETOS, L., MOESTRUP, ., HANSEN, P.J. & DAUGBJERG, GARC N. 2010. The toxic dinoagellate Dinophysis acuminata harbors permanent chloroplasts of cryptomonad origin, not kleptochloroplasts. Harmful Algae 9, 2538. , F. 2012. A checklist and classication of living dinoagGOMEZ ellates (Dinoagellata, Alveolata). CICIMAR Oce anides 27, 65140. -GARC , F., LOPEZ IA, P. & MOREIRA, D. 2009a. Molecular GOMEZ phylogeny of the ocelloid-bearing dinoagellates Erythropsidinium and Warnowia (Warnowiaceae, Dinophyceae). Journal of Eukaryotic Microbiology 56, 440445. -GARC , F., LOPEZ IA, P., NOWACZYK, A. & MOREIRA, D. GOMEZ 2009b. The crustacean parasites Ellobiopsis Caullery, 1910 and Thalassomyces Niezabitowski, 1913 form a monophyletic divergent clade within the Alveolata. Systematic Parasitology 74, 6574. -GARC , F., MOREIRA, D. & LOPEZ IA, P. 2009c. Life cycle GOMEZ and molecular phylogeny of the dinoagellates Chytriodinium and Dissodinium, ectoparasites of copepod eggs. European Journal of Protistology 45, 260270. -GARC , F., MOREIRA, D. & LOPEZ IA, P. 2010a. Neoceratium GOMEZ gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist 161, 3554. -GARC GOMEZ , F., MOREIRA, D. & LOPEZ IA, P. 2010b. Molecular phylogeny of noctilucoid dinoagellates (Noctilucales, Dinophyta). Protist 161, 466478. GUILLOU, L., VIPREY, M., CHAMBOUVET, A., WELSH, R.M., KIRKHAM, A.R., MASSANA, R., SCANLAN, D.J. & WORDEN, A.Z. 2008. Widespread occurrence and genetic diversity of marine parasitoids belonging to Syndiniales (Alveolata). Environmental Microbiology 10, 33493365. HACKETT, J.D., ANDERSON, D.M., ERDNER, D.L. & BHATTACHARYA, D. 2004. Dinoagellates: A remarkable evolutionary experiment. American Journal of Botany 91, 15231534. HANSEN, P.J. 2011. The role of photosynthesis and food uptake for the growth of marine mixotrophic dinoagellates. Journal of Eukaryotic Microbiology 58, 203214. HERDMAN, E.C. 1924. Notes on dinoagellates and other organisms causing discolouration of the sand at Port Erin. IV. Transactions of the Liverpool Biological Society 38, 7584. JEONG, H.J., YEONG, D.Y., PARK, J.Y., SONG, J.Y., KIM, S.T., LEE, S.H., KIM, K.Y. & YIH, W.H. 2005. Feeding by phototrophic red-tide dinoagellates: ve species newly revealed and six species previously known to be mixotrophic. Aquatic Microbial Ecology 40, 133150. LAJEUNESSE, T. 2002. Diversity and community structure of symbiotic dinoagellates from Caribbean coral reefs. Marine Biology 141, 387400. LAJEUNESSE, T.C., LAMBERT, G., ANDERSON, R.A., COFFROTH, M.A. & GALBRAITH, D.W. 2005. Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoagellates. Journal of Phycology 41, 880886. LIN, S. 2011. Genomic understanding of dinoagellates. Research in Microbiology 162, 551569. LOGARES, R., SHALCHIAN-TABRIZI, K., BOLTOVSKOY, A. & RENGEFORS, K. 2007. Extensive dinoagellate phylogenies

dinoagellates is underestimated. The coloured dinoagellates 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 dinoagellate is highly heterogeneous. Because of their ecological and evolutionary importance, dinoagellates 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 oor.

Acknowledgements
F.G. is supported by the contract JCI-2010-08492 of the Ministerio Espa nol de Ciencia y Tecnolog a.

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Associate Editor: Elliot Shubert