Species boundaries in the toxic dinoflagellate prorocentrum lima (Dinophyceae, Prorocentrales), based on morphological and phylogenetic characters

Journal of Phycology

Volumn 47, Issue 1, 2011, Pages 178-189

  Nagahama, Yukio ^a   Murray, Shauna ^b   Tomaru, Akiko ^a   Fukuyo, Yasuwo ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

DSP; ITS; Prorocentrum; Prorocentrum arenarium; Prorocentrum lima; RDNA; Species boundary; Taxonomy

Indexed keywords

DINOPHYCEAE; PROROCENTRALES; PROROCENTRUM; PROROCENTRUM ARENARIUM; PROROCENTRUM LIMA;

EID: 79951784832     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2010.00939.x     Document Type: Article

References (70)

1. Aligizaki, K. & Nikolaidis, G. 2006. The presence of the potentially toxic genera Ostreopsis and Coolia (Dinophyceae) in the North Aegean Sea, Greece. Harmful Algae 5:717-30.
2. Aligizaki, K., Nikolaidis, G., Katikou, P., Bazevanis, A. D. & Abatzopoulos, T. J. 2008. Potentially toxic epiphytic Prorocentrum (Dinophyceae) species in Greek coastal waters. Harmful Algae 8:299-311.
3. Bomber, J. W., Norris, D. R. & Mitchell, E. 1985. Benthic dinoflagellates associated with ciguatera from the Florida Keys. II. Temporal, spatial and substrate heterogeneity of Prorocentrum lima. In Anderson, D. M., White, A. W. & Baden, D. G. [Eds.] Toxic Dinoflagellates. Elsevier Scientific, New York, pp. 45-50.
4. Bouaïcha, B., Chézeau, A., Turquet, J., Quod, J.-P. & Puiseux-Dao, S. 2001. Morphological and toxicological variability of Prorocentrum lima clones isolated from four locations in the south-west Indian Ocean. Toxicon 39:1195-202.
5. Bravo, I. 1991. Results of preliminary studies in the field and in culture of the toxic dinoflagellate Prorocentru lima (Ehrenberg) Dodge. Rev. Int. Oceanogr. Med. 109:189-96.
6. Bütschli, O. 1885. Erster Band. Protozoa. In Bronn, H. G. [Ed.] Klassenund Ordnungen des Thier-Reichs, Wissenschaftlich Dargestellt in Wort und Bild. C. F. Winter'sche Verlagshandlung, Leipzig, Germany, pp. 865-1088.
7. Carlson, R. D. & Tindall, D. R. 1985. Distribution and periodicity of toxic dinoflagellates in the Virgin Islands. In Anderson, D. M., White, A. W. & Baden, D. G. [Eds.] Toxic Dinoflagellates. Elsevier Scientific, New York, pp. 171-6.
8. Carter, N. 1938. New or interesting algae from brackish water. Arch. Protistenk. 90:1-68.
9. Catherine, B., Benoit, B., Bernard, R., Mariaam, R. & Frederic., I. 1995. Phytoplankton time-series data of the French phyto-plankton monitoring network. In Lassus, P., Erard, E. & Marcaillou, C. [Eds.] Harmful Marine Algal Blooms. Lavoisier, Paris, pp. 771-6.
10. Delgado, G., Popowski, G. & Nodar, R. 2000. Primer reporte de Prorocentrum lima (Ehr) Dodge 1975, en aguas Cubanas. Rev. Investig. Mar. 21:103-5.
11. Dodge, J. D. 1965. Thecal fine-structure in the dinoflagellate genera Prorocentrum and Exuviaella. J. Mar. Biol. Assoc. U. K. 45:607-14.
12. Dodge, J. D. 1975. The Prorocectrales (Dinophyceae). II. Revision of the taxonomy within the genus Prorocentrum. Bot. J. Linn. Soc. 71:103-25.
13. Dodge, J. D. 1982. Marine Dinoflagellates of the British Isles. Her Majesty's Stationery Office, London, 303 pp.
14. Dodge, J. D. & Bibby, B. T. 1973. The Prorocentrales (Dinophyceae). I. A comparative account of fine structure in the genera Prorocentrum and Exuviaella. Bot. J. Linn. Soc. 67:175-83.
15. Ehrenberg, C. 1860. Nachtrag zu Hrn. Ehrenbergs Mittheilung vom 8. Decbr. 1859. Verzeichniss der Leuchtthierchen. Monatsberichte der Königlichen Preussischen Akad. Wiss. Berl. 1859:791-3.
16. Ehrenberg, C. 1873. Die das Funkeln und Ausblitzen des Mittelmeeres bewirkenden unsichtbar kleinen Lebensformen. Ges. Naturforsch. Freunde Berl. Festschrift Feier Hundertjährigen Bestehens 1873:1-4.
17. Faust, M. A. 1991. Morphology of ciguatera-causing Prorocentrum lima (Pyrrophyta) from widely differing sites. J. Phycol. 27:642-8.
18. Faust, M. A. 1993. Sexuality in a toxic dinoflagellate, Prorocentrum lima. In Smayda, T. J. & Shimizu, Y. [Eds.] Toxic Phytoplankton Blooms in the Sea. Elsevier Scientific, New York, pp. 121-6.
19. Faust, M. A. 1994. Three new benthic species of Prorocentrum (Dinophyceae) from Carrie Bow Cay, Belize: P. sabulosum sp. nov., P. sculptile sp. nov., and P. arenarium sp. nov. J. Phycol. 30:755-63.
20. Felsenstein, J. 1989. PHYLIP- Phylogeny Inference Package (Version 3.2). Cladistics 5:164-6.
21. Fensome, R. A., Taylor, F. J. R., Norris, G., Sarfeant, W. A. S., Wharton, D. I. & Williams, G. L. 1993. Division dinoflagellata. In Couvering, J. V. & Dinkins, G. [Eds.] A Classification of Living and Fossil Dinoflagellates. Sheridan Press, Pennsylvania, 351 pp.
22. France, J. 2006. Diversity and some ecological aspects of armored dinoflagellates in the Gulf of Trieste, the Adriatic Sea. Period. Biol. 108:159-68.
23. Fukuyo, Y. 1981. Taxonomical study on benthic dinoflagellates collected in coral reefs. Bull. Jpn. Soc. Sci. Fish. 47:967-78.
24. Gayoso, A. M., Dover, S., Morton, S., Busman, M., Moeller, P., Fulco, V. K. & Maranda, L. 2002. Diarrhetic shellfish poisoning associated with Prorocentrum lima (Dinophyceae) in Patagonian Gulfs (Argentina). J. Shellfish Res. 21:461-3.
25. Grzebyk, D., Berland, B., Thomassin, B. A., Bosi, C. & Arnoux, A. 1994. Ecology of ciguateric dinoflagellates in the coral reef complex of Mayotte Island (S.W. Indian Ocean). J. Exp. Mar. Biol. Ecol. 178:51-66.
26. 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. 34:1055-68.
27. Heil, C. A., Maranda, L. & Shimizu, Y. 1993. Mucus-associated dinoflagellates: large scale culturing and estimation of growth rate. In Smayda, T. J. & Shimizu, Y. [Eds.] Toxic Phytoplankton Blooms in the Sea. Elsevier Scientific, New York, pp. 501-6.
28. Heredia-Tapia, A., Arredondo-Vega, B. O., Nuñes-Vázquez, E. J., Yasumoto, T., Yasuda, M. & Ochoa, J. L. 2002. Isolation of Prorocentrum lima (Syn. Exuviaella lima) and diarrhetic shellfish poisoning (DSP) risk assessment in the Gulf of California, Mexico. Toxicon 40:1121-7.
29. Hoppenrath, M. 2000. A new marine sand-dwelling Prorocentrum species, P. clipeus sp. nov. (Dinophyceae, Prorocentrales) from Helgoland, German Bight, North Sea. Eur. J. Protistol. 36:29-33.
30. Imamura, K. & Fukuyo, Y. 1987. Observation of armoured dinoflagellates. In Fukuyo, Y., Takano, H., Chihara, M. & Matsuoka, K. [Eds.] A Guide for Studies of Red Tide Organisms. Japan Fisheries Resource Conservation Association, Tokyo, pp. 64-72.
31. Jow, H., Hudelot, C., Rattray, M. & Higgs, P. G. 2002. Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol. Biol. Evol. 19:1591-601.
32. Keller, M., Selvin, R. C., Claus, W. & Guillard, R. R. L. 1987. Media for the culture of oceanic ultraphytoplankton. J. Phycol. 23:633-8.
33. Klebs, G. 1884. Ein kleiner Beitrag zur Kenntnis der Peridineen. Bot. Z. 42:734-45.
34. Koike, K., Sato, S., Yamaji, M., Nagahama, Y., Kotaki, Y., Ogata, T. & Kodama, M. 1998. Occurrence of okadaic acid-producing Prorocentrum lima on the Sanriku Coast, Northern Japan. Toxicon 36:2039-42.
35. Landsberg, J. H., Balazs, G. H., Steidinger, K. A., Baden, D. G., Work, T. M. & Russell, D. J. 1999. The potential role of natural tumor promoters in marine turtle fibropapillomatosis. J. Aquat. Anim. Health 11:199-210.
36. Lebour, M. V. 1925. The Dinoflagellates of the Northern Seas. Marine Biological Association of the United Kingdom, Plymouth, UK, 250 pp.
37. Levasseur, M., Couture, J.-Y., Weise, A. M., Michaud, S., Elbrächter, M., Sauvé, G. & Bonneau, E. 2003. Pelagic and epiphytic summer distributions of Prorocentrum lima and P. mexicanum at two mussel farms in the Gulf of St. Lawrence, Canada. Aquat. Microb. Ecol. 30:283-93.
38. Maranda, L., Chan, C. & Martin, C. 1999. Prorocentrum lima (Dinophyceae) in waters of the Great South Channel near Georges Bank. J. Phycol. 35:1158-61.
39. Maranda, L., Keller, M. D., Hurst, J. W., Bean, L. L., Mcgowan, J. D. & Hargraves, P. E. 2000. Spatio-temporal distribution of Prorocentrum lima in coastal waters of the Gulf of Maine: a two-year survey. J. Shellfish Res. 19:1003-6.
40. Marasigan, A. N., Tamse, A. F. & Fukuyo, Y. 2001. Prorocentrum (Prorocentrales: Dinophyceae) populations on seaglass-blade surface in Taklong Island, Guimaras Province, Philippines. Plankton Biol. Ecol. 48:79-84.
41. Marr, J. C., Jackson, A. E. & McLachlan, J. L. 1992. Occurrence of Prorocentrum lima, a DSP toxin-producing species from the Atlantic coast of Canada. J. Appl. Phycol. 4:17-25.
42. McLachlan, J. L., Boalch, G. T. & Jahn, R. 1997. Reinstatement of the genus Exuviaella (Dinophyceae, Prorocentrophycidae) and an assessment of Prorocentrum lima. Phycologia 36:38-46.
43. Mohammad-Noor, N., Daugbjerg, N., Moestrup, Ø. & Anton, A. 2006. Marine epibenthic dinoflagellates from Malaysia - a study of live cultures and preserved samples based on light and scanning electron microscopy. Nord. J. Bot. 24:629-90.
44. Morton, S. L. & Faust, M. A. 1997. Survey of toxic epiphytic dinoflagellates from the Belizean barrier reef ecosystem. Bull. Mar. Sci. 61:899-906.
45. Morton, S. L., Norris, D. R. & Bomber, J. W. 1992. Effect of temperature, salinity and light intensity on the growth and seasonality of toxic dinoflagellates associated with ciguatera. J. Exp. Mar. Biol. Ecol. 157:79-90.
46. Morton, S. L. & Tindall, D. R. 1995. Morphological and biochemical variability of the toxic dinoflagellate Prorocentrum lima isolated from three locations at Heron Island, Australia. J. Phycol. 31:914-21.
47. Murakami, Y., Oshima, Y. & Yasumoto, T. 1982. Identification of okadaic acid as a toxic component of a marine dinoflagellate Prorocentrum lima. Bull. Jpn. Soc. Sci. Fish. 48:69-72.
48. Nagahama, Y. & Fukuyo, Y. 2005. Redescription of Cryptomonas lima, collected from Sorrento, Italy, the basionym of Prorocentrum lima. Plankton Biol. Ecol. 52:107-9.
49. Nascimento, S. M., Purdie, D. A. & Morris, S. 2005. Morphology, toxin composition and pigment content of Prorocentrum lima strains isolated from a coastal lagoon in southern UK. Toxicon 45:633-49.
50. Ogata, T., Kodama, M. & Ishimaru, T. 1987. Toxin production in the dinoflagellate Protogonyaulax tamarensis. Toxicon 25:923-8.
51. Okolodkov, Y. B., Campos-Bautista, G., Gárate-Lizárraga, I., González-González, J. G., Hoppenrath, M. & Arenas, V. 2007. Seasonal change of benthic and epiphytic dinoflagellates in the Veracruz reef zone, Gulf of Mexico. Aquat. Microb. Ecol. 47:223-7.
52. Paulsen, O. 1908. Peridiniales. In Brandt, K. & Apstein, C. [Eds.] Nordisches Plankton. Verlag von Lipsius & Tischer, Leipzig, Germany, pp. XVIII 5-6.
53. Pearce, I., Marshall, J.-A. & Hallegraeff, G. M. 2000. Toxic epiphytic dinoflagellates from East Coast Tasmania, Australia. In Hallegraeff, G. M., Blackburn, S. I., Bolch, C. J. & Lewis, R. J. [Eds.] Harmful Algal Blooms 2000. UNESCO 2001, Fontenoy, France, pp. 54-7.
54. Piyakarnchana, T., Wissessang, S., Pholpunthin, P., Phadung, Y. & Rungsupa, S. 1986. Dinoflagellates and diatoms on the surface of the seven species of corals. Galaxea 5:123-8.
55. Posada, D. & Crandall, K. A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-8.
56. Posada, D. & Crandall, K. A. 2001. Selecting the best-fit model of nucleotide substitution. Syst. Biol. 50:580-601.
57. Praseno, D. P. & Wiadnyana, N. N. 1996. HAB organisms in Indonesian waters. Can. Tech. Rep. Fish. Aquat. Sci. 2138:69-75.
58. Quod, J. P., Turquet, J., Diogene, G. & Fessard, V. 1995. Screening of extracts of dinoflagellates from coral reefs (Reunion Island, SW Indian Ocean), and thier biological activities. In Lassus, P., Erard, E. & Marcaillou, C. [Eds.] Harmful Marine Algal Blooms. Lavoisier, Paris, pp. 815-20.
59. Rhodes, L. L. & Syhre, M. 1995. Okadaic acid production by a New Zealand Prorocentrum lima isolate. New Zealand. J. Mar. Freshw. Res. 29:367-70.
60. Schiller, J. 1933. Dinoflagellatae (Peridineae) in monographischer Behandlung. Part 1. In Rabenhorst, L. [Ed.] Kryptogamen-Flora von Deutschland. Österreich und der Schweiz, Zehnter Band, Flagellata, Dritte Abteilung. Akademische Verlagsgesllschaft M.B.H., Leipzig, Germany, pp. 16-45.
61. Schütt, F. 1896. Peridiniales. In Engler, A. & Prantl, K. [Eds.] Die natürlichen Pelanzen Familien nebst ihren Gattungen und wichtigeren Arten, insbesondere den Nutzpflanzen, unter Mitwirkung zahlreicher hervorragender Fachgelehrten. I. teil. 1. Abteilung b: Gymnodiniaceae, Prorocentraceae, Peridiniaceae, Bacillariaceae. Verlag von Wilhelm Engelmann, Leipzig, Germany, fig. 9.
62. Stein, F. R. 1878. Der Organismus der Infusionsthiere nach eigenen forschungen in systematischer reihenfolge bearbeitet. III. Abtheilung, I. Hälfte. In Engelmann, W. [Ed.] Die Naturgeschichte der Flagellaten Order Geisselinfusorien. Leipzig, Germany, pp. 70-3.
63. Stein, F. R. 1883. Der Organismus der Infusionsthiere nach eigenen Forschungen in systematischer Reihenfloge bearbeitet. III. Abteilung, II. Hälfte. In Engelmann, W. [Ed.] Die Naturgeschichte der Arthrodelen Flagellaten. Wilhelm Engelmann, Leipzig, Germany, pp. 8-17, Tafel I.
64. Swofford, D. L. 2000. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, Massachusetts.
65. Taylor, F. J. R. 1980. On dinoflagellate evolution. Biosystems 13:65-108.
66. Thompson, J. D., Higgins, D. G. & Gibson, T. J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-80.
67. Tomas, C. R. & Baden, D. G. 1993. The influence of phosphorus on the growth and cellular toxin content of the benthic dinoflagellate Prorocentrum lima. In Smayda, T. J. & Shimizu, Y. [Eds.] Toxic Phytoplankton Blooms in the Sea. Elsevier Scientific, New York, pp. 565-70.
68. Turki, S. 2005. Distribution of toxic dinoflagellates along the leaves of seagrass Posidonia oceanica and Cymodocea nodosa from the Gulf of Tunis. Cah. Biol. Mar. 46:29-34.
69. Vila, M., Garcés, E. & Masó, M. 2001. Potentially toxic epiphytic dinoflagellate assemblages on macroalgae in the NW Mediterranean. Aquat. Microb. Ecol. 26:51-60.
70. Yoo, J. S. 2004. Morphological variation of dinoflagellate Prorocentrum lima (Ehrenberg) Dodge with geographical difference. J. Environ. Biol. 25:51-8.