Abstract
The so-called unarmoured dinoflagellates are not a “natural” (phylogenetic) group but they lack thecal plates, share fragility and possess relatively few morphological characters that can be positively identified. This study depicts the species composition of unarmoured dinoflagellates collected from sites along the coasts of the Gulf of Mexico and the Mexican Pacific and includes their descriptions and illustrations. We identified a total of 25 species belonging to 13 genera and six families that were studied through various techniques using light and scanning electron microscopy. Seven new records for the Mexican Pacific are annotated here that include Amphidinium flagelans Schiller, Gyrodinium cochlea Lebour, G. glaebum Hulburt, G. metum Hulburt, Karenia selliformis Haywood, Steidinger et MacKenzie, Karlodinium ballantinum de Salas, and K. veneficum (Ballantine) Larsen. The genera Karenia and Karlodinium belong to the family Kareniaceae, characterised for encompassing the largest number of toxic species among the unarmoured dinoflagellates, and many species produce algal blooms around the world. Ceratoperidinium falcatum and Levanderina fissa are names recently proposed elsewhere as new taxonomic combinations and are also included here. The diversity of unarmoured dinoflagellates has been strongly underestimated in the past and the new records reported here confirm this. Further studies, including traditional and modern concepts and protocols (including molecular tools), should be undertaken in the near future to understand their real diversity.
About the authors
Sergio Escobar-Morales is a biologist from the Universidad Juárez Autónoma de Tabasco (UJAT) who obtained his MSc degree from the Universidad Nacional Autónoma de México (UNAM). He is presently working at the Centro de Investigación Científica de Yucatán, A.C. in Cancún, Mexico. He has been studying the dinoflagellate community in both planktonic and benthic realms in the Mexican Pacific, the Gulf of Mexico and the Caribbean Sea.
David U. Hernández-Becerril obtained his degrees: Biologist from the Universidad Nacional Autónoma de México (UNAM), MSc from CICESE, and PhD from the University of Bristol, UK. He has been a titular researcher at the Instituto de Ciencias del Mar y Limnología, UNAM for more than 18 years and studies marine phytoplankton mainly biodiversity, taxonomy and ecology of the whole community and also particular taxonomic groups such as diatoms, dinoflagellates, coccolithophores, silicoflagellates and other smaller groups in Mexican waters, describing some new species. He has published about 100 peer-reviewed papers, four books and 12 book chapters. He has been the direct supervisor of 25 theses for BA, MSc and PhD degrees.
Acknowledgments
We appreciate SEM facilities given by Yolanda Hornelas. Thanks are also due to A. Morales-Blake, Flora Colin and S. Barón-Campis for supplying samples, and A. Monreal and M.L. Machaín for their invitations to participate in their oceanographic expeditions (DIPAL-II and TEHUA-V bis, respectively). Special thanks are given to Karen Steidinger, M. de Salas and Santiago Fraga for their help in identifying members of Kareniaceae. S.E.-Morales received a postgraduate fellowship from CONACYT and also partial support PAPIIT, DGAPA, Universidad Nacional Autónoma de México (Project No. IN226209-3).
References
Alonso-Rodríguez, R., J.L. Ochoa and M. Uribe-Alcocer. 2005. Grazing of heterotrophic dinoflagellate Noctiluca scintillans (Macartney) Kofoid on Gymnodinium catenatum Graham. Rev. Lat.-Amer. Microbiol. 47: 6–10.Search in Google Scholar
Bergholtz, T., N. Daugbjerg and Ø. Moestrup. 2005. On the identity of Karlodinium veneficum and description of Karlodinium armiger sp. nov. (Dinophyceae), based on light and electron microscopy, nuclear-encoded LSU rDNA, and pigment composition. J. Phycol. 42: 170–193.Search in Google Scholar
Bolch, J.S.C., P.A. Negri and G.M. Hallegraeff. 1999. Gymnodinium microreticulatum sp. nov. (Dinophyceae): a naked microreticulate cyst-producing dinoflagellate, distinct from Gymnodinium catenatum and Gymnodinium nolleri. Phycologia38: 301–313.Search in Google Scholar
Botes, L., B. Price, M. Waldron and G.C. Pitcher. 2002. A simple and rapid scanning electron microscope preparative technique for delicate “Gymnodinioid” Dinoflagellates. Microsc. Res. Tech. 59: 128–130.10.1002/jemt.10184Search in Google Scholar PubMed
Botes, L., S.D. Sym and G.C. Pitcher. 2003. Karenia cristata sp. nov. and Karenia bicuneiformis sp. nov. (Dinophysiales, Dinophyceae): two new Karenia species from the South African coast. Phycologia 42: 563–571.Search in Google Scholar
Chang, F.H. and K.G. Ryan. 2004. Karenia concordia sp. nov. (Gymnodiniales, Dinophyceae), a new nonthecate dinoflagellate isolated New Zealand northeast during the 2002 harmful algal bloom events. Phycologia 43: 552–562.Search in Google Scholar
Daugbjerg, N., G. Hansen, J. Larsen and Ø. Moestrup. 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 unarmored dinoflagellates. Phycologia 39: 302–317.Search in Google Scholar
de Salas, M.F., C. Bolch, L. Botes, G. Nash, S.W. Wright and G.M. Hallegraeff. 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.Search in Google Scholar
de Salas, M.F., C.J.F. Bolch and G.M. Hallegraeff. 2004a. Karenia asterichroma sp. nov. (Gymnodiniales, Dinophyceae), a new dinoflagellate species associated with finfish aquaculture mortalities in Tasmania, Australia. Phycologia 43: 624–631.10.2216/i0031-8884-43-5-624.1Search in Google Scholar
de Salas, M.F., C.J.F. Bolch and G.M. Hallegraeff. 2004b. Karenia umbella sp. nov. (Gyrnnodiniales, Dinophyceae), a new potentially ichthyotoxic dinoflagellate species from Tasmania, Australia. Phycologia 43: 166–175.Search in Google Scholar
de Salas, M.F., A. Laza-Martínez and G.M. Hallegraeff. 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: 241–257.10.1111/j.1529-8817.2007.00458.xSearch in Google Scholar PubMed
Faust, M.A. and R.A. Gulledge. 2002. Identifying harmful marine dinoflagellates. Smithsonian Contr. U.S. Natl. Herb.42: 1–144.Search in Google Scholar
Fensome, R.A., F.J.R. Taylor, G. Norris, W.A.S. Sarjeant, D.J. Wharton and G.I. Williams. 1993. A classification of living and fossil dinoflagellates. Micropaleontology, Special Publishers. No. 7, Sheridan Press, Hanover. pp. 351.Search in Google Scholar
Flø Jørgensen, M.F., S. Murray and N. Daugbjerg. 2004. Amphidinium revisited. I. Redefinition of Amphidinium (Dinophyceae) based on cladistic and molecular phylogenetic analyses. J. Phycol. 40: 351–365.10.1111/j.1529-8817.2004.03131.xSearch in Google Scholar
Garcés, E., M. Fernández, A. Penna, K. Van Lenning, A. Gutierrez, J. Camp and M. Zapata. 2006. Characterization of NW Mediterranean Karlodinium spp. (Dinophyceae) strains using morphological, molecular, chemical and physiological methodologies. J. Phycol. 42: 1096–1112.Search in Google Scholar
Gómez, F. 2007. Gymnodinioid dinoflagellates (Gymnodiniales, Dinophyceae) in the open Pacific Ocean. Algae22: 273–286.Search in Google Scholar
Gómez, F. 2013. Morphology and distribution of Pronoctiluca (Dinoflagellata, incertae sedis) in the Pacific Ocean. Acta Oceanol. Sin. 32: 71–76.Search in Google Scholar
Guillard, R.R.L. and P.E. Hargraves. 1993. Stichochrysis immobilis is a diatom, not a Chrysophyte. Phycologia32: 234–236.Search in Google Scholar
Hallegraeff, G.M., J.S.C. Bolch, J.M. Huisman and M.F. de Salas. 2010. Planktonic dinoflagellates. In: (G.M. Hallegraeff, J.S.C. Bolch, D.R.A. Hill, I. Jameson, J.-M. Le Poi, A. McMinn, S. Murray, M.F. de Salas and K. Sanders, eds). Algae of Australia. Phytoplankton of temperate coastal waters. Australia Biological Resources Study (ABRS), Canberra; CSIRO Publishing, Melbourne. pp. 145–212.Search in Google Scholar
Hansen, G. and J. Larsen. 1992. Dinoflagellater i danske farvande. In: (H.A. Thomsen, ed) Plankton i de indre danske farvande. Havforskning fra Miljøstyrelsen. Milijøministeriet Miljøstyrelsen. pp. 45–155.Search in Google Scholar
Haywood, A.J., K.A. Steidinger and E.W. Truby. 2004. Comparative morphology and molecular phylogenetic analysis of three new species of the genus Karenia (Dinophyceae) from New Zealand. J. Phycol. 40: 165–179.10.1111/j.0022-3646.2004.02-149.xSearch in Google Scholar
Hernández-Becerril, D.U., R. Alonso-Rodríguez, C. Álvarez-Gongora, S.A. Barón-Campis, G. Ceballos-Corona, J. Herrera-Silveira, M.E. Meave del Castillo, N. Juárez-Ruíz, F. Merino-Virgilio, A.R. Morales-Blake, J.L. Ochoa, E. Orellana-Cepeda, C. Ramírez-Camarena and R. Rodríguez-Amador. 2007. Toxic and harmful marine phytoplankton and microalgae (HABs) in Mexican Coasts. J. Environ. Sci. HealthA. 42: 1349–1363.10.1080/10934520701480219Search in Google Scholar PubMed
Hoppenrath, M. and B.S. Leander. 2007. Character evolution in Polykrikoid dinoflagellates. J.Phycol. 43: 366–377.10.1111/j.1529-8817.2007.00319.xSearch in Google Scholar
Hoppenrath, M., N. Yubuki, T.R. Bachvaroff and B.S. Leander. 2010. Re-classification of Pheopolykrikos hartmanii as Polykrikos (Dinophyceae) based partly on the ultrastructure of complex extrusomes. Eur. J. Protistol. 46: 29–37.10.1016/j.ejop.2009.08.003Search in Google Scholar PubMed
Hulburt, E.M. 1957. The taxonomy of unarmored Dinophyceae of shallow embayments on Cape Cod, Massachussetts. Biol. Bull. 112: 196–219.10.2307/1539198Search in Google Scholar
Kofoid, C.A. and O. Swezy. 1921. The free living unarmored dinoflagellata. Memoirs of the University of California, Berkeley, USA. pp. 563.Search in Google Scholar
Larsen, J. 2002. Dinoflagelados atecados potencialmente toxígenos en el cono sur Americano. In: (E.A. Sar, M.E. Ferrario and B. Reguera, eds). Floraciones Algales Nocivas en el Cono Sur Americano. Instituto Español de Oceanografía, Madrid, Spain. pp. 147–154.Search in Google Scholar
Larsen, J. and N.L. Nguyen. 2004. Gymnodiniales. In: (J. Larsen and N.L. Nguyen, eds). Potentially toxic microalgae of Vietnamese waters. Opera Botanica, Copenhagen, Denmark. 140, pp. 117–125.Search in Google Scholar
Licea, S., M.E. Zamudio, R. Luna and J. Soto. 2004. Free living dinoflagellates in the southern Gulf of México: Report of data (1979–2002). Phycol. Res. 52: 419–428.10.1111/j.1440-1835.2004.tb00351.xSearch in Google Scholar
Maciel-Baltazar, E. and D.U. Hernández-Becerril. 2013. Especies de dinoflagelados atecados (Dinophyta) de la costa de Chiapas, sur del Pacífico mexicano. Rev. Biol. Mar. Oceanogr. 48: 245–259.Search in Google Scholar
Margalef, R. 1961. Hidrografía y fitoplancton de un área marina de la costa meridional de Puerto Rico. Invest. Pesq. 18: 33–96.Search in Google Scholar
Matsuoka, K. and Y. Fukuyo. 1986. Cyst and motile morphology of a colonial dinoflagellate Pheopolykrikos hartmanii (Zimmermann) comb. nov. J. PlanktonRes. 8: 818–896.10.1093/plankt/8.4.811Search in Google Scholar
Matsuoka, K., M. Iwataki and H. Kawami. 2008. Morphology and taxonomy of chain-forming species of the genus Cochlodinium (Dinophyceae). Harmful Algae 7: 261–270.10.1016/j.hal.2007.12.002Search in Google Scholar
Moestrup, Ø. and N. Daugbjerg. 2007. On dinoflagellate phylogeny and classification. In: (J. Brodies and J. Lewis, eds). Unraveling the algae, the past, present, and future of algal systematics. CRC Press, New York. pp. 215–230.Search in Google Scholar
Moestrup, Ø., P. Hakanen, G. Hansen, N. Daugbjerg and M. Ellegaard. 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.Search in Google Scholar
Monreal-Gómez, M.A. and D.A. Salas de León. 1997. Circulación y estructura termohalina del Golfo de México. In: (M.F. Lavin, ed). Contribuciones a la oceanografía física en México. Monografía N° 3. Unión Geofísica Mexicana. Ensenada, B.C. México. pp. 183–199.Search in Google Scholar
Ojeda, A. 2005. Dinoflagelados de Canarias. Estudio taxonómico y ecológico. Monografías LXV. Instituto de Estudios Canarios, Tenerife, Spain. pp. 301.Search in Google Scholar
Okolodkov, Y.B. and I. Gárate-Lizárraga. 2006. An annotated checklist of dinoflagellates (Dinophyceae) from the Mexican Pacific. Acta Bot. Mex. 74: 1154.10.21829/abm74.2006.1008Search in Google Scholar
Orr, R.J.S., S.A. Murray, A. Stüken, L. Rhodes and K.S. Jakobsen. 2012. When naked became armored: an eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS ONE7: e5004.10.1371/journal.pone.0050004Search in Google Scholar
Reñé, A., M. de Salas, J. Camp, V. Balagué and E. Garcés. 2013. A new clade, based on partial LSU rDNA sequence, of unarmored dinoflagellates. Protist 164: 673–685.Search in Google Scholar
Reñé, A., J. Camp and E. Garcés. 2014. Polykrikos tanit sp. nov., a new mixotrophic unarmored pseudocolonial dinoflagellates from the NW Mediterranean Sea. Protist 165: 81–92.Search in Google Scholar
Schiller, J. 1933. Dinoflagellatae (Peridineae). In: (L. Rabenhorst, ed), Dr. L. Rabenhorst’s. Kryptogamen-flora von Deutschland, Österreich und der Schweiz. 10.3 (I), Akad. Verlag, Leipzig, pp. 590.Search in Google Scholar
Siano, R., W.H.C.F. Kooistra, M. Montresor and A. Zingone. 2009. Unarmoured and thin-walled dinoflagellates from the Gulf of Naples, with the description of Woloszynskia cincta sp. nov. (Dinophyceae, Suessiales). Phycologia 48: 44–65.10.2216/08-61.1Search in Google Scholar
Steidinger, K. and K. Tangen. 1997. Dinoflagellates. In: (C.R. Tomas, ed). Identifying marine phytoplankton. Academic Press, San Diego, USA. pp. 387–584.Search in Google Scholar
Steidinger, K., J.L. Wolny and A.J. Haywood. 2008. Identification of Kareniaceae (Dinophyceae) in the Gulf of Mexico. Nova Hedwigia 133: 269–284.Search in Google Scholar
Takayama, H. 1985. Apical grooves of unarmoured dinoflagellates. Bull. PlanktonSoc. Jpn. 32: 129–140.Search in Google Scholar
Tang, Y.Z., M.J. Harke and C.J. Gobler. 2013. Morphology, phylogeny, dynamics, and ichthyotoxicity of Pheopolykrikos hartmannii (Dinophyceae) isolates and blooms from New York, USA. J. Phycol. 49: 1084–1094.10.1111/jpy.12114Search in Google Scholar
Taylor, F.J.R. 1976. Dinoflagellates from the International Indian Ocean Expedition. Bibliotheca Botanica 132: 1–234.Search in Google Scholar
Taylor, F.J.R., Y. Fukuyo, J. Larsen and G.M. Hallegraeff. 2003. Taxonomy of harmful dinoflagellates. In: (G.M. Hallegraeff, D.M. Anderson and A.D. Cembella, eds). Manual on harmful marine microalgae. Monogr. Oceanogr. Methodol., UNESCO Pub. Academic Press, Paris, France. pp. 389–432.Search in Google Scholar
Truby, E.W. 1997. Preparation of single-celled marine dinoflagellates for electron microscopy. Microsc. Res. Tech. 36: 337–340.10.1002/(SICI)1097-0029(19970215)36:4<337::AID-JEMT11>3.0.CO;2-QSearch in Google Scholar
Zingone, A. and H.O. Enevoldsen. 2000. The diversity of harmful algal blooms: a challenge for science and management. Ocean Coast. Manage. 43: 725–748.10.1016/S0964-5691(00)00056-9Search in Google Scholar
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