Skip to main content
SpringerLink
Log in

Dinoflagellate taxonomy — a review and proposal of a revised classification

  • Review
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

The knowledge about morphology-based taxonomy and classification as well as molecular phylogenetic hypotheses and character evolution of dinokaryotic dinoflagellates was summarized. Recommendations for future taxonomic work and character evaluations were given. A classification scheme based on nameless ranked systematics for dinoflagellate levels above genus was proposed. Higher ranks were based on the relative number of alveolae (Polyalveolate and Oligoalveolate) and their arrangement. Polyalveolate had alveolae arranged in series or not. Oligoalveolate had alveolae arranged in different tabulation patterns (Symmetricomorpha, Asymmetricomorpha, Sagittale). A group of taxa with unclear tabulation type (in-between peridinioid and gonyaulacoid) was separated and named Mesomorpha. A higher rank for taxa with a sagittal suture splitting only the hyposome in two lateral halves (extra tabulation pattern) was created, Pre-sagittale. The classification intended to highlight the unresolved relationships of higher ranks. Furthermore, the difficulties to define characters suitable for general higher rank circumscription should become visible. The study pinpointed what needs to be done to improve the current dinoflagellate taxonomy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CR, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup Ø, Mozley-Standridge SE, Nerad TS, Shearer CA, Smirnov AV, Spiegel FW, Taylor FJR (2005) The new high level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451

    Article  PubMed  Google Scholar 

  • Adl SM, Leander BS, Simpson AGB, Archibald JM, Anderson OR, Bass D, Bowser SS, Brugerolle G, Farmer MA, Karpov S, Kolisko M, Lane CE, Lodge DJ, Mann DG, Meisterfeld R, Mendoza L, Moestrup Ø, Mozley-Standridge SE, Smirnov AV, Spiegel F (2007) Diversity, nomenclature, and taxonomy of protists. Syst Biol 56:684–689

    Article  PubMed  Google Scholar 

  • Adl SM, Simpson AGB, Lane CR, Lukes J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, Le Gall L, Lynn DH, McManus H, Mitchell EAD, Mozley-Stanridge SE, Parfrey LW, Pawlowski J, Rückert S, Shadwick L, Schoch CL, Smirnov A, Spiegel FW (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Bachvaroff TR, Gornik SG, Concepcion GT, Waller RF, Mendez GS, Lippmeier JC, Delwiche CF (2014) Dinoflagellate phylogeny revisited: using ribosomal proteins to resolve deep branching dinoflagellate clades. Mol Phyl Evol 70:314–322

    Article  CAS  Google Scholar 

  • Balech E (1979) El género Pyrophacus Stein (Dinoflagellata). Physis 38(94):27–38

    Google Scholar 

  • Biecheler B (1952) Recherches sur les péridiniens. Bull Biol France Belgique, Suppl 36:1–149

    Google Scholar 

  • Bourrelly P (1970) Les algues d’eau douce. Initiation à la systématique. Tome III: Les algues bleues et rouges. Les Eugléniens, Peridiniens et Cryptomonadines. Éditions N. Boubée and Cie, Paris

    Google Scholar 

  • Bujak JP, Williams GL (1981) The evolution of dinoflagellates. Can J Bot 59:2077–2087

    Article  Google Scholar 

  • Carlos AA, Baillie BK, Kawachi M, Maruyama T (1999) Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free-living strain. J Phycol 35:1054–1062

    Article  CAS  Google Scholar 

  • Cavalier-Smith T (1993) Kingdom Protozoa and its 18 phyla. Microbiol Rev 57:953–994

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cavalier-Smith T, Chao EE (2004) Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur J Protistol 40:185–212

    Article  Google Scholar 

  • Chomérat N, Couté A, Nézan E (2010) Further investigations on the sand-dwelling genus Cabra (Dinophyceae, Peridiniales) in South Brittany (northwestern France), including the description of C. aremorica sp. nov. Mar Biodivers 40:131–142

    Article  Google Scholar 

  • Claparède E, Lachmann J (1859) Ètude sur les infusoires et les rhizopodes. Inst Ntnl Génevois Mémoires 6:261–482

    Google Scholar 

  • Clarke KJ, Pennick NC (1972) Flagellar scales in Oxyrrhis marina Dujardin. Br Phycol J 7:357–360

    Article  Google Scholar 

  • Clarke KJ, Pennick NC (1976) The occurrence of body scales in Oxyrrhis marina Dujardin. Br Phycol J 11:345–348

    Article  Google Scholar 

  • Coats DW (1988) Dubosquella cachoni n. sp., a parasitic dinoflagellate lethal to its tintinnine host Eutintinnus pectinis. J Protozool 35:607–617

    Article  Google Scholar 

  • Coats DW (1999) Parasitic life styles of marine dinoflagellates. J Eukaryot Microbiol 46:402–409

    Article  Google Scholar 

  • Coats DW, Bachvaroff TR, Delwiche CF (2012) Revision of the family Dubosquellidae with description of Eudubosquella crenulata n. gen., n. sp. (Dinoflagellata, Syndinea), an intracellular parasite of the ciliate Favella panamensis Kofoid & Campbell, 1929. J Eukaryot Microbiol 59:1–11

    Article  PubMed  Google Scholar 

  • Craveiro SC, Moestrup Ø, Daugbjerg N, Calado AJ (2010) Ultrastructure and large subunit rDNA-based phylogeny of Sphaerodinium cracoviense, an unusual freshwater dinoflagellate with a novel type of eyespot. J Eukaryot Microbiol 57:568–585

    Article  CAS  PubMed  Google Scholar 

  • Darling KF, Wade CM, Kroon D, Leigh Brown AJ (1997) Planktic foraminiferal molecular evolution and their polyphyletic origins from benthic taxa. Mar Micropaleontol 30:251–266

    Article  Google Scholar 

  • Daugbjerg N, Hansen G, Larsen J, Moestrup Ø (2000) Phylogeny of some of the major genera of dinoflagellates based on ultrastructure and partial LSU rDNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302–317

    Article  Google Scholar 

  • De Salas MF, Bolch CJS, Botes L, Nash G, Wright SW, Hallegraeff GM (2003) Takayama gen. nov. (Gymnodiniales, Dinophyceae), a new genus of unarmored dinoflagellates with sigmoid apical grooves, including the description of two new species. J Phycol 39:1233–1246

    Article  Google Scholar 

  • De Salas MF, Bolch CJS, Hallegraeff GM (2004) Karenia umbella sp. nov. (Gymnodiniales, Dinophyceae), a new potentially ichthyotoxic dinoflagellate species from Tasmania, Australia. Phycologia 43:166–175

    Article  Google Scholar 

  • De Salas MF, Laza-Martínez A, Hallegraeff GM (2008) Novel unarmored dinoflagellates from the toxigenic family Kareniaceae (Gymnodiniales): five new species of Karlodinium and one new Takayama from the Australian sector of the Southern Ocean. J Phycol 44:241–257

    Article  PubMed  CAS  Google Scholar 

  • Diéz B, Pedros-Alio C, Massana R (2001) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl Env Microbiol 67:2932–2941

    Article  Google Scholar 

  • Dodge JD, Crawford RM (1971) A fine-structural survey of dinoflagellate pyrenoids and food-reserves. Bot J Linn Soc 64:105–115

    Article  Google Scholar 

  • Dodge JD, Hermes HB (1981) A scanning electron microscopical study of the apical pores of marine dinoflagellates (Dinophyceae). Phycologia 20:424–430

    Article  Google Scholar 

  • Edvardsen B, Shalchian-Tabrizi K, Jakobsen KS, Medlin LK, Dahl E, Brubak S, Paasche E (2003) Genetic variability and molecular phylogeny of Dinophysis species (Dinophyceae) from Norwegian waters inferred from single cell analyses of rDNA. J Phycol 39:395–408

    Article  CAS  Google Scholar 

  • Ehrenberg CG (1838) Die Infusionsthierchen als volkommene Organismen. Ein Blick in das Tiefere organische Leben der Natur. Leopold Voss, Leipzig, 547 pp

    Book  Google Scholar 

  • Elbrächter M, Gottschling M, Hildebrand-Habel T, Keupp H, Kohring R, Lewis J, Meier KJS, Montresor M, Streng M, Versteegh GJM, Willems H, Zonneveld K (2008) Establishing an agenda for calcareous dinoflagellate research (Thoracosphaeraceae, Dinophyceae) including a nomenclatural synopsis of generic names. Taxon 57:1289–1303

    Google Scholar 

  • Fast NM, Xue L, Bingham S, Keeling PJ (2002) Re-examining alveolate evolution using multiple protein molecular phylogenies. J Eukaryot Microbiol 49:30–37

    Article  CAS  PubMed  Google Scholar 

  • Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL (1993) A classification of living and fossil dinoflagellates. Am Mus Nat Hist Micropaleontol Spec Publ Num 7:1–351

    Google Scholar 

  • Fensome RA, MacRae RA, Moldowan JM, Taylor FJR, Williams GL (1996) The early Mesozoic radiation of dinoflagellates. Paleobiology 22:329–338

    Article  Google Scholar 

  • Fensome RA, Saldarriaga JF, Taylor FJR (1999) Dinoflagellate phylogeny revisited: reconciling morphological and molecular based phylogenies. Grana 38:66–80

    Article  Google Scholar 

  • Figueroa RI, Garcés E, Bravo I (2007) Comparative study of the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture. J Phycol 43:1039–1053

    Article  Google Scholar 

  • Figueroa RI, Rengefors K, Bravo I, Bensch S (2010) From homothally to heterothally: mating preferences and genetic variation within clones of the dinoflagellate Gymnodinium catenatum. Deep-Sea Res II 57:190–198

    Article  CAS  Google Scholar 

  • Flø Jørgensen M, Murray S, Daugbjerg N (2004a) Amphidinium revisited. I. Redefinition of Amphidinium (Dinophyceae) based on cladistic and molecular phylogenetic analyses. J Phycol 40:351–365

    Article  Google Scholar 

  • Flø Jørgensen M, Murray S, Daugbjerg N (2004b) A new genus of athecate interstitial dinoflagellates, Togula gen. nov., previously encompassed within Amphidinium sensu lato: Inferred from light and electron microscopy and phylogenetic analyses of partial large subunit ribosomal DNA sequences. Phycol Res 52:284–299

    Article  Google Scholar 

  • Fukuda Y, Endoh H (2006) New details from the complete life cycle of the red-tide dinoflagellate Noctiluca scintillans (Ehrenberg) McCartney. Eur J Protistol 42:209–219

    Article  PubMed  Google Scholar 

  • Fukuda Y, Endoh H (2008) Phylogenetic analyses of the dinoflagellate Noctiluca scintillans based on ß-tubulin and Hsp90 genes. Eur J Protistol 44:27–33

    Article  PubMed  Google Scholar 

  • Garcés E, Hoppenrath M (2010) Ultrastructure of the intracellular parasite Parvilucifera sinerae (Alveolata, Myzozoa) infecting the marine toxic planktonic dinoflagellate Alexandrium minutum (Dinophyceae). Harmful Algae 10:64–70

    Article  Google Scholar 

  • Gómez F (2005) A list of dinoflagellates in the world oceans. Acta Bot Croatica 84:129–212

    Google Scholar 

  • Gómez F (2013) Problematic biases in the availability of molecular markers in protists: the example of the dinoflagellates. Acta Protozool 52:21–33

    Google Scholar 

  • Gómez F, López-García P, Moreira D (2009) Molecular phylogeny of the ocelloid-bearing dinoflagellates Erythropsidinium and Warnowia (Warnowiaceae, Dinophyceae). J Eukaryot Microbiol 56:440–445

    Article  PubMed  CAS  Google Scholar 

  • Gómez F, Moreira D, López-García P (2010) Molecular phylogeny of noctilucoid dinoflagellates (Noctilucales, Dinophyceae). Protist 161:466–478

    Article  PubMed  CAS  Google Scholar 

  • Greuet C (1987) Complex organelles. In: Taylor FJR (ed.) The biology of dinoflagellates. Botanical Monographs 21. Blackwell, Oxford, pp 119–142

    Google Scholar 

  • Gribble KE, Anderson DM (2006) Molecular phylogeny of the heterotrophic dinoflagellates, Protoperidinium, Diplopsalis and Preperidinium (Dinophyceae), inferred from large subunit rDNA. J Phycol 42:1081–1095

    Article  Google Scholar 

  • Gribble KE, Anderson DM (2007) High intraindividual, intraspecific, and interspecific variability in large-subunit ribosomal DNA in the heterotrophic dinoflagellates Protoperidinium, Diplopsalis and Preperidinium (Dinophyceae). Phycologia 46:315–324

    Article  Google Scholar 

  • Grzebyk D, Sako Y, Berland B (1998) Phylogenetic analysis of nine species of Prorocentrum (Dinophyceae) inferred from 18S ribosomal DNA sequences, morphological comparisons, and description of Prorocentrum panamensis sp. nov. J Phycol 34:1055–1068

    Article  CAS  Google Scholar 

  • Gu H, Liu T, Mertens KN (2015) Cyst–theca relationship and phylogenetic position of Protoperidinium (Peridiniales, Dinophyceae) species of the sections Conica and Tabulata, with description of Protoperidinium shanghaiense sp. nov. Phycologia 54:49–66

    Article  Google Scholar 

  • Handy SM, Bachvaroff TR, Timme RE, Coats DW, Kim S, Delwiche CF (2009) Phylogeny of four dinophysiacean genera (Dinophyceae, Dinophysiales) based on rDNA sequences from single cells and environmental samples. J Phycol 45:1163–1174

    Article  CAS  PubMed  Google Scholar 

  • Hansen G, Daugbjerg N (2011) Moestrupia oblonga gen. & comb. nov. (syn.: Gyrodinium oblongum), a new marine dinoflagellate genus characterized by light and electron microscopy, photosynthetic pigments and LSU rDNA sequence. Phycologia 50:583–599

    Article  CAS  Google Scholar 

  • Hansen G, Daugbjerg N, Franco JM (2003) Morphology, toxin composition and LSU rDNA phylogeny of Alexandrium minutum (Dinophyceae) from Denmark, with some morphological observations on other European strains. Harmful Algae 2:317–335

    Article  CAS  Google Scholar 

  • Hansen G, Botes L, de Salas M (2007) Ultrastructure and large subunit rDNA sequences of Lepidodinium viride reveal a close relationship to Lepidodinium chlorophorum comb. nov. (= Gymnodinium chlorophorum). Phycol Res 55:25–41

    Article  CAS  Google Scholar 

  • Harada A, Ohtsuka S, Horiguchi T (2007) Species of the parasitic genus Duboscquella are members of the enigmatic marine alveolate group I. Protist 158:337–347

    Article  CAS  PubMed  Google Scholar 

  • Hastrup Jensen M, Daugbjerg N (2009) Molecular phylogeny of selected species of the order Dinophysiales (Dinophyceae) — testing the hypothesis of a dinophysioid radiation. J Phycol 45:1136–1152

    Article  Google Scholar 

  • Höhfeld I, Melkonian M (1995) Ultrastructure of the flagellar apparatus of Noctiluca miliaris Suriray swarmers (Dinophyceae). Phycologia 34:508–513

    Article  Google Scholar 

  • Hoppenrath M (2000a) Morphology and taxonomy of six marine sand-dwelling Amphidiniopsis species (Dinophyceae, Peridiniales), four of them new, from the German Bight, North Sea. Phycologia 39:482–497

    Article  Google Scholar 

  • Hoppenrath M (2000b) An emended description of Herdmania litoralis Dodge (Dinophyceae) including the plate formula. Nova Hedwigia 71:481–489

    Google Scholar 

  • Hoppenrath M, Elbrächter M (2015) Center of Excellence for Dinophyte Taxonomy (CEDiT). http://www.dinophyta.org/

  • Hoppenrath M, Leander BS (2007a) Character evolution in polykrikoid dinoflagellates. J Phycol 43:366–377

    Article  Google Scholar 

  • Hoppenrath M, Leander BS (2007b) Morphology and phylogeny of the pseudocolonial dinoflagellates Polykrikos lebourae and Polykrikos herdmanae n. sp. Protist 158:209–227

    Article  CAS  PubMed  Google Scholar 

  • Hoppenrath M, Leander BS (2008) Morphology and molecular phylogeny of a new marine sand-dwelling Prorocentrum species, P. tsawwassenensis sp. nov. (Dinophyceae, Prorocentrales), from British Columbia, Canada. J Phycol 44:451–466

    Article  PubMed  Google Scholar 

  • Hoppenrath M, Leander BS (2009) Molecular phylogeny of Parvilucifera prorocentri (Alveolata, Myzozoa): insights into perkinsid character evolution. J Eukaryot Microbiol 56:251–256

    Article  CAS  PubMed  Google Scholar 

  • Hoppenrath M, Leander BS (2010) Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences. PLoS ONE 5, e13220

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoppenrath M, Saldarriaga JF (2008) ToLweb dinoflagellate page. http://tolweb.org/Dinoflagellates/2445

  • Hoppenrath M, Schweikert M, Elbrächter M (2003) Morphological reinvestigation and characterisation of the marine, sand-dwelling dinoflagellate Adenoides eludens (Dinophyceae). Eur J Phycol 38:385–394

    Article  Google Scholar 

  • Hoppenrath M, Horiguchi T, Miyoshi Y, Selina M, Taylor FJR, Leander BS (2007) Taxonomy, phylogeny, biogeography, ecology of Sabulodinium undulatum, including an amended description of the species. Phycol Res 55:159–175

    Article  Google Scholar 

  • Hoppenrath M, Elbrächter M, Drebes G (2009) Marine phytoplankton. Selected microphytoplankton species from the North Sea around Helgoland and Sylt. Kleine Senckenberg-Reihe 49. Schweizerbart Science, Stuttgart, p 264

    Google Scholar 

  • Hoppenrath M, Bachvaroff TR, Handy SM, Delwiche CF, Leander BS (2009b) Molecular phylogeny of ocelloid-bearing dinoflagellates (Warnowiaceae) as inferred from SSU and LSU rDNA sequences. BMC Evol Biol 9:116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hoppenrath M, Yubuki N, Bachvaroff TR, Leander BS (2010) Reclassification of Pheopolykrikos hartmannii as Polykrikos (Dinophyceae) based partly on the ultrastructure of complex extrusomes. Eur J Protistol 46:29–37

    Article  PubMed  Google Scholar 

  • Hoppenrath M, Murray S, Sparmann SF, Leander BS (2012) Morphology and molecular phylogeny of Ankistrodinium gen. nov. (Dinophyceae), a new genus of marine sand-dwelling dinoflagellates formerly classified within Amphidinium. J Phycol 48:1143–1152

    Article  PubMed  Google Scholar 

  • Hoppenrath M, Chomérat N, Horiguchi T, Schweikert M, Nagahama Y, Murray SA (2013a) Taxonomy and phylogeny of the benthic Prorocentrum species (Dinophyceae) — a proposal and review. Harmful Algae 27:1–28

    Article  Google Scholar 

  • Hoppenrath M, Chomérat N, Leander BS (2013b) Molecular phylogeny of Sinophysis: evaluating the possible early evolutionary history of dinophysoid dinoflagellates. In: Lewis JM, Marret F, Bradley L (eds) Biological and geological perspectives of dinoflagellates. The Micropalaeontological Society, Special Publications. Geological Society, London, pp 207–214

    Google Scholar 

  • Hoppenrath M, Murray SA, Chomérat N, Horiguchi T (2014) Marine benthic dinoflagellates — unveiling their worldwide biodiversity. Kleine Senckenberg-Reihe 54, Schweizerbart Science, Stuttgart, p 276

    Google Scholar 

  • Horiguchi T, Sukigara C (2005) Pyramidodinium atrofuscum gen. et sp. nov. (Dinophyceae), a new marine sand-dwelling coccoid dinoflagellate from tropical waters. Phycol Res 53:247–254

    Article  Google Scholar 

  • Horiguchi T, Yoshizawa-Ebata J, Nakayama T (2000) Halostylodinium arenarium, gen. et sp. nov. (Dinophyceae), a coccoid sand-dwelling dinoflagellate from subtropical Japan. J Phycol 36:960–971

    Article  Google Scholar 

  • Horiguchi T, Tamura M, Katsumata K, Yamaguchi A (2012) Testudodinium gen. nov. (Dinophyceae), a new genus of sand-dwelling dinoflagellates formerly classified in the genus Amphidinium. Phycol Res 60:137–149

    Article  Google Scholar 

  • Iwataki M, Hansen G, Sawaguchi T, Hiroishi S, Fukuyo Y (2004) Investigation of body scales in twelve Heterocapsa species (Peridiniales, Dinophyceae), including a new species H. pseudotriquetra sp. nov. Phycologia 43:394–403

    Article  Google Scholar 

  • Iwataki M, Hansen G, Moestrup Ø, Matsuoka K (2010) Ultrastructure of the harmful unarmored dinoflagellate Cochlodinium polykrikoides (Dinophyceae) with reference to the apical groove and flagellar apparatus. J Eukaryot Microbiol 57:308–321

    Article  PubMed  Google Scholar 

  • John U, Litaker RW, Montresor M, Murray S, Brosnahan ML, Anderson DM (2014) Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165:779–804

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang NS, Jeong HJ, Moestrup Ø, Shin W, Nam SW, Park JY, DeSalas MF, Kim KW, Noh JH (2010) Description of a new planktonic mixotrophic dinoflagellate Paragymnodinium shiwhaense n. gen., n. sp. from coastal waters off western Korea: morphology, pigments, and ribosomal DNA gene sequence. J Eukaryot Microbiol 57:121–144

    Article  CAS  PubMed  Google Scholar 

  • Kang NS, Jeong HJ, Moestrup Ø, Park TG (2011) Gyrodiniellum shiwhaense n. gen., n. sp., new planktonic heterotrophic dinoflagellate from the coastal waters of western Korea: morphology and ribosomal DNA gene sequence. J Eukaryot Microbiol 58:284–309

    Article  PubMed  Google Scholar 

  • Ki J-S (2010) Nuclear 28S rDNA phylogeny supports the basal placement of Noctiluca scintillans (Dinophyceae; Noctilucales) in dinoflagellates. Eur J Protistol 46:111–120

    Article  PubMed  Google Scholar 

  • Kofoid CA, Skogsberg T (1928) The Dinoflagellata: the Dinophysoidae. Harvard University, Museum of Comparative Zoology, Memoirs 51:708 pp

  • Kofoid CA, Swezy O (1921) The free-living unarmored Dinoflagellata. University of California, Memoirs 5:562 pp

  • Kuvardina ON, Leander BS, Aleshin VV, Mylnikov AP, Keeling PJ, Simdyanov TG (2002) The phylogeny of colpodellids (Alveolata) using small-subunit rRNA gene sequences suggests they are the free-living sister group to apicomplexans. J Eukaryot Microbiol 49:498–504

    Article  CAS  PubMed  Google Scholar 

  • LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiontic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880

    Article  CAS  Google Scholar 

  • LaJeunesse TC, Parkinson JE, Reimer JD (2012) A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria. J Phycol 48:1380–1391

    Article  PubMed  Google Scholar 

  • Larsen J, Patterson DJ (1990) Some flagellates (Protista) from tropical marine sediments. J Nat Hist 24:801–937

    Article  Google Scholar 

  • Leander BS, Hoppenrath M (2008) Ultrastructure of a novel tube-forming, intracellular parasite of dinoflagellates: Parvilucifera prorocentri sp. nov. (Alveolata, Myzozoa). Eur J Protistol 44:55–70

    Article  PubMed  Google Scholar 

  • Leander BS, Keeling PJ (2003) Morphostasis in alveolate evolution. Trends Ecol Evol 18:395–402

    Article  Google Scholar 

  • Leander BS, Keeling PJ (2004) Early evolutionary history of dinoflagellates and apicomplexans (Alveolata) as inferred from hsp90 and actin phylogenies. J Phycol 40:341–350

    Article  CAS  Google Scholar 

  • Leaw CP, Lim PT, Ng BK, Cheah MY, Ahmad A, Usup G (2005) Phylogenetic analysis of Alexandrium species and Pyrodinium bahamense (Dinophyceae) based on theca morphology and nuclear ribosomal gene sequence. Phycologia 44:550–565

    Article  Google Scholar 

  • Lim P-T, Leaw CP, Ogata T (2007) Morphological variation of two Alexandrium species responsible for paralytic shellfishnpoisoning in Southeast Asia. Bot Mar 50:14–21

    Article  Google Scholar 

  • Lindberg K, Moestrup Ø, Daugbjerg N (2005) Studies on woloszynskioid dinoflagellates I: Woloszynskia coronata re-examined using light and electron microscopy and partial LSU rDNA sequences, with description of Tovellia gen. nov. and Jadwigia gen. nov. (Tovelliaceae fam. nov.). Phycologia 44:416–440

    Article  Google Scholar 

  • Litaker RW, Tester P, Colorni A, Levy MG, Noga EJ (1999) The phylogenetic relationship of Pfiesteria piscicida, cryptoperidiniopsoid sp. Amyloodinium ocellatum and a Pfiesteria-like dinoflagellate to other dinoflagellates and apicomplexans. J Phycol 35:1379–1389

    Article  Google Scholar 

  • Liu T, Gu H, Mertens KN, Lan D (2014) New dinoflagellate species Protoperidinium haizhouense sp. nov. (Peridiniales, Dinophyceae), its cyst-theca relationship and phylogenetic position within the Monovela group. Phycol Res 62:109–124

    Article  CAS  Google Scholar 

  • Logares R, Rengefors K, Kremp A, Shalchian-Tabrizi K, Boltovskoy A, Tengs T, Shurtleff A, Klaveness D (2007a) Phenotypically different microalgal morphospecies with identical ribosomal DNA: a case of rapid adaptive evolution? Microb Ecol 53:549–561

    Article  CAS  PubMed  Google Scholar 

  • Logares R, Schalchian-Tabrizi K, Boltovskoy A, Rengefors K (2007b) Extensive dinoflagellate phylogenies indicate infrequent marine–freshwater transitions. Mol Phylogenet Evol 45:887–903

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Garcia P, Rodriguez-Valera F, Pedros-Alio C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607

    Article  CAS  PubMed  Google Scholar 

  • Lowe CD, Montagnes DJS, Martin LE, Watts PC (2010) Patterns of genetic diversity in the marine heterotrophic flagellate Oxyrrhis marina (Alveoloata: Dinophyceae). Protist 161:212–221

    Article  CAS  PubMed  Google Scholar 

  • Lundholm N, Moestrup Ø (2006) The biogeography of harmful algae. In: Granelli E, Turner JT (eds) Ecology of harmful algae. Ecological Studies 189. Springer, Heidelberg, pp 23–35

    Chapter  Google Scholar 

  • Maroteaux L, Herzog M, Soyer-Gobillard MO (1985) Molecular organization of dinoflagellate ribosomal DNA: molecular implications of the deduced 5.8S rRNA secondary structure. Biosystems 18:307–319

    Article  CAS  PubMed  Google Scholar 

  • Matsuoka K, Kawami H, Fujii R, Iwataki M (2006) Further examination of the cyst-theca relationship of Protoperidinium thulesense (Peridiniales, Dinophyceae) and the phylogenetic significance of round brown cysts. Phycologia 45:632–641

    Article  Google Scholar 

  • Mertens KN, Yamaguchi A, Takano Y, Pospelova V, Head MJ, Radi T, Pienkowski AJ, de Vernal A, Kawami H, Matsuoka K (2013) A new heterotrophic dinoflagellate from the north-eastern Pacific, Protoperidinium fukuyoi: cyst-theca relationship, phylogeny, distribution and ecology. J Eukaryot Microbiol 60:545–563

    Article  CAS  PubMed  Google Scholar 

  • Moestrup Ø, Daugbjerg N (2007) On dinoflagellate phylogeny and classification. In: Brodie J, Lewis J (eds) Unravelling the algae — the past, present, and future of algal systematics. The Systematics Association Special Volume Series 75, CRC Press, Boca Raton, pp 215–230

    Chapter  Google Scholar 

  • Moestrup Ø, Hansen G, Daugbjerg N, Flaim G, D’Andrea M (2006) Studies on woloszynskioid dinoflagellates II: on Tovellia sanguinea sp. nov., the dinoflagellate responsible for the redding of Lake Tovel. N Italy Eur J Phycol 41:47–65

    Article  Google Scholar 

  • Moestrup Ø, Hansen G, Daugbjerg N (2008) Studies on woloszynskioid dinoflagellates III: on the ultrastructure and phylogeny of Borghiella dodgei gen. et sp. nov., a cold-water species from Lake Tovel, N. Italy, and on B. tenuissima comb. nov. (syn. Woloszynskia tenuissima). Phycologia 47:54–78

    Article  CAS  Google Scholar 

  • Moestrup Ø, Lindberg K, Daugbjerg N (2009a) Studies on woloszynskioid dinoflagellates IV: the genus Biecheleria gen. nov. Phycol Res 57:203–220

    Article  Google Scholar 

  • Moestrup Ø, Lindberg K, Daugbjerg N (2009b) Studies on woloszynskioid dinoflagellates V: ultrastructure of Biecheleriopsis gen. nov., with description of Biecheleriopsis adratica sp. nov. Phycol Res 57:221–237

    Article  CAS  Google Scholar 

  • Moestrup Ø, Hakanen P, Hansen G, Daugbjerg N, Ellegaard M (2014) On Levanderina fissa gen. & comb. nov. (Dinophyceae) (syn. Gymnodinium fissum, Gyrodinium instriatum, Gyr. uncatenum), a dinoflagellate with a very unusual sulcus. Phycologia 53:265–292

    Article  Google Scholar 

  • Montresor M, Sgrosso S, Procaccini G, Kooistra WHCF (2003) Intraspecific diversity in Scrippsiella trochoidea (Dinophyceae): evidence for cryptic species. Phycologia 42:56–70

    Article  Google Scholar 

  • Moreira D, López-García P (2002) The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol 10:31–38

    Article  CAS  PubMed  Google Scholar 

  • Murray S (2003) Diversity and phylogenetics of sand-dwelling dinoflagellates from southern Australia. PhD thesis, School of Biological Sciences, University of Sydney, pp. 202

  • Murray S, Patterson DJ (2004) Cabra matta, gen. nov., sp. nov., a new benthic, heterotrophic dinoflagellate. Eur J Phycol 39:229–234

    Article  Google Scholar 

  • Murray S, Flø Jørgensen M, Ho SYW, Patterson DJ, Jermiin LS (2005) Improving the analysis of dinoflagellate phylogeny based on rDNA. Protist 156:269–286

    Article  CAS  PubMed  Google Scholar 

  • Murray S, Hoppenrath M, Preisfeld A, Larsen J, Yoshimatsu S, Toriumi S, Patterson DJ (2006) Phylogenetics of Rhinodinium broomeense gen. et sp. nov., a peridinoid, sand-dwelling dinoflagellate (Dinophyceae). J Phycol 42:934–942

    Article  CAS  Google Scholar 

  • Murray S, Ip CL-C, Moore R, Nagahama Y, Fukuyo Y (2009) Are prorocentroid dinoflagellates monophyletic? A study of 25 species based on nuclear and mitochondrial genes. Protist 160:245–264

    Article  CAS  PubMed  Google Scholar 

  • Nagahama Y, Murray S, Tomaru A, Fukuyo Y (2011) Species boundaries in the toxic dinoflagellate Prorocentrum lima (Dinophyceae, Prorocentrales) based on morphological and phylogenetic characters. J Phycol 47:178–189

    Article  PubMed  Google Scholar 

  • Orr RJS, Murray SA, Stüken A, Rhodes L, Jakobsen KS (2012) When naked became armoured: an eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS ONE 7(11), e50004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patterson DJ (1986) Some problems of ambiregnal taxonomy and a possible solution. Symp Biol Hung 33:87–91

    Google Scholar 

  • Patterson DJ (1999) The diversity of eukaryotes. Am Nat 154:96–124

    Article  Google Scholar 

  • Patterson DJ, Larsen J (1991) Chapter 24. Nomenclatural problems with protists. In: Hawksworth DL (ed.) Improving the stability of names: needs and opinions. Regnum Vegetabile No. 123. Koeltz, Königstein, pp 197–208

    Google Scholar 

  • Patterson DJ, Larsen J (1992) A perspective on protistan nomenclature. J Protozool 39:125–131

    Article  Google Scholar 

  • Pfiester LA, Anderson DM (1987) Dinoflagellate reproduction. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 611–648

    Google Scholar 

  • Popovský J, Pfiester LA (1990) Dinophyceae (Dinoflagellida). Süßwasser-Flora von Mitteleuropa Band 6. Gustav Fischer Verlag, Jena, p 272

    Google Scholar 

  • Round FE, Crawford RM (1981) The lines of evolution of the Bacillariophyta. I. Origin. Proc R Soc Lond 211:237–260

    Article  Google Scholar 

  • Saldarriaga JF, Taylor FJR, Keeling PJ, Cavalier-Smith T (2001) Dinoflagellate nuclear SSU rRNA phylogeny suggests multiple plastid losses and replacements. J Mol Evol 53:204–213

    Article  CAS  PubMed  Google Scholar 

  • Saldarriaga JF, McEwan ML, Fast NM, Taylor FJR, Keeling PJ (2003) Multiple protein phylogenies show that Oxyrrhis marina and Perkinsus marinus are early branches of the dinoflagellate lineage. Int J Syst Evol Microbiol 53:355–365

    Article  CAS  PubMed  Google Scholar 

  • Saldarriaga JF, Taylor FJR, Cavalier-Smith T, Menden-Deuer S, Keeling PJ (2004) Molecular data and the evolutionary history of dinoflagellates. Eur J Protistol 40:85–111

    Article  Google Scholar 

  • Sampedro N, Fraga S, Penna A, Casabianca S, Zapata M, Grünewald CF, Riobó P, Camp J (2011) Barrufeta bravensis gen. nov. sp. nov. (Dinophyceae): a new bloom-forming species from the northwest Mediterranean Sea. J Phycol 47:375–392

    Article  PubMed  Google Scholar 

  • Saunders GW, Hill DRA, Sexton JP, Andersen RA (1997) Small-subunit ribosomal RNA sequences from selected dinoflagellates: testing classical evolutionary hypotheses with molecular systematic methods. Pl Syst Evol 11:237–259

    Article  CAS  Google Scholar 

  • Schnepf E, Drebes G (1993) Anisogamy in the dinoflagellate Noctiluca? Helgoländer Meeresun 47:65–273

    Article  Google Scholar 

  • Schnepf E, Elbrächter M (1992) Nutritional strategies in dinoflagellates: a review with emphasis on cell biological aspects. Eur J Protistol 28:3–24

    CAS  PubMed  Google Scholar 

  • Schnepf E, Elbrächter M (1999) Dinophyte chloroplasts and phylogeny — a review. Grana 38:81–97

    Article  Google Scholar 

  • Selina M, Hoppenrath M (2008) An emended description of Amphidiniopsis arenaria Hoppenrath 2000, based on material from the Sea of Japan. Eur J Protistol 44:71–79

    Article  PubMed  Google Scholar 

  • Shalchian-Tabrizi K, Minge MA, Cavalier-Smith T, Nedreklepp JM, Klaveness D, Jakobsen KS (2006) Combined heat shock protein 90 and ribosomal RNA sequence phylogeny supports multiple replacements of dinoflagellate plastids. J Eukaryot Microbiol 53:217–224

    Article  CAS  PubMed  Google Scholar 

  • Silberman JD, Collins AG, Gershwin LA, Johnson PJ, Roger AJ (2004) Ellobiopsids of the genus Thalassiomyces are alveolates. J Eukaryot Microbiol 51:246–252

    Article  PubMed  Google Scholar 

  • Sims PA, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45:361–402

    Article  Google Scholar 

  • Skovgaard A, Massana R, Balagué V, Saiz E (2005) Phylogenetic position of the copepod-infesting parasite Syndinium turbo (Dinoflagellata, Syndinea). Protist 156:413–423

    Article  CAS  PubMed  Google Scholar 

  • Skovgaard A, Massana R, Saiz E (2007) Parasitic species of the genus Blastodinium (Blastodiniphyceae) are peridinioid dinoflagellates. J Phycol 43:553–560

    Article  Google Scholar 

  • Slamovits CH, Saldarriaga JF, Larocque A, Keeling PJ (2007) The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both apicomplexan and dinoflagellate mitochondrial genomes. J Mol Biol 372:356–388

    Article  CAS  PubMed  Google Scholar 

  • Soehner S, Zinßmeister C, Kirsch M, Gottschling M (2012) Who am I – and if so, how many? Species diversity of calcareous dinophytes (Thoracosphaeraceae, Peridiniales) in the Mediterranean Sea. Org Divers Evol 12:339–348

    Article  Google Scholar 

  • Sparmann SF, Leander BS, Hoppenrath M (2008) Comparative morphology and molecular phylogeny of taxa of the new marine benthic dinoflagellate genus Apicoporus, classified formerly within Amphidinium sensu lato. Protist 159:383–399

    Article  PubMed  Google Scholar 

  • von Stein FR (1883) Der Organismus der Infusionsthiere nach eigenen Forschungen in systematischer Reihenfolge bearbeitet. III. Abteilung, II. Hälfte. Die Naturgeschichte der arthrodelen Flagellaten. Wilhelm Engelmann, Leipzig, 30 pp., 25 pl

    Google Scholar 

  • Stern RF, Horak A, Andrew RL, Coffroth M-A, Andersen RA, Küpper FC, Jameson I, Hoppenrath M, Véron B, Kasai F, Brand J, James ER, Keeling PJ (2010) Environmental barcoding reveals massive dinoflagellate diversity in marine environments. PLoS ONE 5(11), e13991

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS (2006) A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:31–43

    Article  CAS  PubMed  Google Scholar 

  • Tai LS, Skogsberg T (1934) Studies on the Dinophysoidae, marine armored dinoflagellates, of Monterey Bay, California. Arch Protistenkd 82:380–482

    Google Scholar 

  • Takano Y, Yamaguchi H, Inouye I, Moestrup Ø, Horiguchi T (2014) Phylogeny of five species of Nusuttodinium gen. nov. (Dinophyceae), a genus of unarmoured kleptoplastidic dinoflagellates. Protist 165:759–778

    Article  PubMed  Google Scholar 

  • Takishita K, Tsuchiya M, Kawato M, Oguri K, Kitazato H, Maruyama T (2007) Genetic diversity of microbial eukaryotes in anoxic sediment of the saline meromictic lake Namako-ike (Japan): on the detection of anaerobic or anoxic-tolerant lineages of eukaryotes. Protist 158:51–64

    Article  CAS  PubMed  Google Scholar 

  • Tamura M, Takano Y, Horiguchi T (2009) Discovery of a novel type of body scale in the marine dinoflagellate, Amphidinium cupulatisquama sp. nov. (Dinophyceae). Phycol Res 57:304–312

    Article  Google Scholar 

  • Taylor FJR (1980) On dinoflagellate evolution. BioSyst 13:65–108

    Article  CAS  Google Scholar 

  • Taylor FJR (1985) The taxonomy and relationships of red tide flagellates. In: Anderson DM, White AW, Baden DG (eds) Toxic dinoflagellates. Elsevier, Holland, pp 11–26

    Google Scholar 

  • Taylor FJR (ed) (1987) The biology of dinoflagellates. Blackwell, Oxford

    Google Scholar 

  • Taylor FJR (2004) Illumination or confusion? Dinoflagellate molecular phylogenetic data viewed from a primarily morphological standpoint. Phycol Res 52:308–324

    Article  CAS  Google Scholar 

  • Taylor FJR, Sarjeant WAS, Fensome RA, Williams GL (1986) Proposals to standardize the nomenclature in flagellate groups currently treated by both the Botanical and Zoological Codes of Nomenclature. Taxon 35:890–896

    Article  Google Scholar 

  • Taylor FJR, Hoppenrath M, Saldarriaga JF (2008) Dinoflagellate diversity and distribution. Biodivers Conserv 17:407–418

    Article  Google Scholar 

  • Thessen AE, Patterson DJ, Murray SA (2012) The taxonomic significance of species that have only been observed once: the genus Gymnodinium (Dinoflagellata) as an example. PLoS ONE 7(8), e44015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tillmann U, Hoppenrath M (2013) The life-cycle of the heterotrophic dinoflagellate Polykrikos kofoidii. J Phycol 49:298–317

    Article  PubMed  Google Scholar 

  • Tillmann U, Elbrächter M, John U, John U, Cembella A (2009) Azadinium spinosum gen. et sp. nov. (Dinophyceae) identified as a primary producer of azaspiracid toxins. Eur J Phycol 44:63–79

    Article  CAS  Google Scholar 

  • Tillmann U, Elbrächter M, John U, John U, Cembella A (2010) Azadinium obesum (Dinophyceae), a new nontoxic species in the genus that can produce azaspiracid toxins. Phycologia 49:169–182

    Article  Google Scholar 

  • Watanabe MM, Suda S, Inouye I, Sawaguchi T, Chihara M (1990) Lepidodinium viride gen. et sp. nov. (Gymnodiniales, Dinophyta), a green dinoflagellate with a chlorophyll A- and B-containing endosymbiont. J Phycol 26:741–751

    Article  Google Scholar 

  • Yamaguchi A, Kawamura H, Horiguchi T (2006) A further phylogenetic study of the heterotrophic dinoflagellate genus, Protoperidinium (Dinophyceae) based on small and large subunit ribosomal RNA gene sequences. Phycol Res 54:317–329

    Article  CAS  Google Scholar 

  • Yamaguchi A, Hoppenrath M, Pospelova V, Horiguchi T, Leander BS (2011) Molecular phylogeny of the marine sand-dwelling dinoflagellate Herdmania litoralis and an emended description of the closely related planktonic genus Archaeperidinium Jörgensen. Eur J Phycol 46:98–112

    Article  Google Scholar 

  • Zhang H, Bhattacharya D, Lin S (2007) A three-gene dinoflagellate phylogeny suggests monophyly of Prorocentrales and a basal position for Amphidinium and Heterocapsa. J Mol Evol 65:463–474

    Article  CAS  PubMed  Google Scholar 

  • Zingmark RG (1970) Sexual reproduction in the dinoflagellate Noctiluca miliaris Suriray. J Phycol 6:122–126

    Google Scholar 

  • Zinßmeister C, Soehner S, Facher E, Kirsch M, Meier KJS, Gottschling M (2011) Catch me if you can: the taxonomic identity of Scrippsiella trochoidea (F.Stein) A.R.Loebl. (Thoracosphaeraceae, Dinophyceae). Syst Biodivers 9:145–157

    Article  Google Scholar 

Download references

Acknowledgments

For discussions about dinoflagellate characters, classification, and molecular phylogenies, I want to thank in particular Juan Saldarriaga, Shauna Murray, and Urban Tillmann. Nicolas Chomérat helped with correct naming. This manuscript is mainly based on the Habilitation thesis of the author.

Author information

Authors and Affiliations

  1. Senckenberg am Meer, DZMB, Südstrand 44, D-26382, Wilhelmshaven, Germany

    Mona Hoppenrath

Authors
  1. Mona Hoppenrath
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mona Hoppenrath.

Ethics declarations

Conflict of Interest

The author, M. Hoppenrath, declares that she has no conflict of interest.

Funding

None.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed consent

For this type of study, formal consent is not required.

Additional information

Communicated by B. Leander

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hoppenrath, M. Dinoflagellate taxonomy — a review and proposal of a revised classification. Mar Biodiv 47, 381–403 (2017). https://doi.org/10.1007/s12526-016-0471-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-016-0471-8

Keywords

Search

Navigation