Accessible Requires Authentication Published by De Gruyter July 5, 2013

The genus Pseudo-nitzschia (Bacillariophyceae) in Manzanillo and Santiago Bays, Colima, Mexico

María Rivera-Vilarelle, Sonia Quijano-Scheggia, Aramis Olivos-Ortiz, Juan Heberto Gaviño-Rodríguez, Fátima Castro-Ochoa and Alejandro Reyes-Herrera
From the journal Botanica Marina

Abstract

In this study, morphological characters were used to describe the diversity and seasonal variability of the genus Pseudo-nitzschia in a coastal region of the Mexican tropical Pacific Ocean. Eleven species were characterized from cultures and field material: Pseudo-nitzschia americana, Pseudo-nitzschia australis, Pseudo-nitzschia brasiliana, Pseudo-nitzschia delicatissima, Pseudo-nitzschia cf. delicatissima, Pseudo-nitzschia dolorosa, Pseudo-nitzschia cf. fryxelliana, Pseudo-nitzschia micropora, Pseudo-nitzschia multistriata, Pseudo-nitzschia pungens var. aveirensis, and Pseudo-nitzschia subfraudulenta. The maximum diversity and abundance occurred in spring, in parallel with a local upwelling, whereas fewer species were detected in autumn. Among those analyzed, the only species to be detected throughout the year at several stations was P. cf. fryxelliana, whereas the rarest species in the study area was P. americana, which was detected only in the spring.


Corresponding author: María Rivera-Vilarelle, Facultad de Ciencias Marinas, Colima University, Carretera Manzanillo-Barra de Navidad km 20, Col. El Naranjo, C.P. 28860, Manzanillo, Colima, Mexico

We thank J. Reyes Gomez and D. Pozas Zepeda for the microphotography and assistance with the SEM. We also thank the University of Colima for the use of its equipment and facilities and an anonymous reviewer for comments to improve the manuscript. This study was supported by PROMEP/103.5/10/7144 and the project FOMIX COLIMA-2009-C04-122077.

References

Álvarez, G., E. Uribe, S. Quijano-Scheggia, A. López-Rivera, C. Mariño and J. Blanco. 2009. Domoic acid production by Pseudo-nitzschia australis and Pseudo-nitzschia calliantha isolated from North Chile. Harmful Algae8: 938–945. Search in Google Scholar

Amato, A. and M. Montresor. 2008. Morphology, phylogeny, and sexual cycle of Pseudo-nitzschia mannii sp. nov. (Bacillariophyceae): a pseudo-cryptic species within the P. pseudodelicatissima complex. Phycologia47: 487–497. Search in Google Scholar

Amato, A., W.H.C.F. Kooistra, J.H. Levialdi Ghiron, D.G. Mann, T. Pröschold and M. Montresor. 2007. Reproductive isolation among sympatric cryptic species in marine diatoms. Protist158: 193–207. Search in Google Scholar

Bates, S.S. 1998. Ecophysiology and metabolism of ASP toxin production. In: (D.M. Anderson, A.D. Cembella and G.M. Hallegraeff, eds) Physiological ecology of harmful algal blooms. Springer-Verlag, Heidelberg. pp. 405–426. Search in Google Scholar

Bates, S.S., D.L. Garrison and R.A. Horner. 1998. Bloom dynamics and physiology of domoic-acid-producing Pseudo-nitzschia species. In: (D.M. Anderson, A.D. Cembella and G.M. Hallegraeff, eds) Physiological ecology of harmful algal blooms. Springer-Verlag, Heidelberg. pp. 267–292. Search in Google Scholar

Baytut, Ö., Ø. Moestrup, N. Lundholm and A. Gönülol. 2013. Contributions to the diatom flora of the Black Sea from ultrastructural and molecular studies: new records of Skeletonema marinoi, Pseudo-nitzschia pungens var. aveirensis and Chaetoceros tenuissimus for the marine flora of Turkey. Nova Hedwigia96: 427–444. Search in Google Scholar

Bérard-Therriault, L., M. Poulin and L. Bossé. 1999. Guide d’identification du phytoplancton marin de l’estuaire et du golfe du Saint-Laurent incluant également certains protozoaires. Publ. Spéc. Can. Sci. Halieut. Aquat.128: 1–387. Search in Google Scholar

Buck, K.R., L. Uttal-Cooke, C.H. Pilskaln, D.L. Roelke, M.C. Villac, G.A. Fryxell, L. Cifuentes and F.P. Chavez. 1992. Autecology of the diatom Pseudonitzschia australis, a domoic acid producer, from Monterey Bay, California. Mar. Ecol. Prog. Ser.84: 293–302. Search in Google Scholar

Cabrales-Talavera, G. 2010. Distribución espacial y temporal de diatomeas del género Pseudo-nitzschia spp y concentración de ácido domoico en la región de la Bahía de Todos Santos, B.C., México. MS thesis. Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE), Ensenada. pp. 88. Search in Google Scholar

Cho, E.S., Y. Kotaki and J.G. Park. 2001. The comparison between toxic Pseudo-nitzschia multiseries (Hasle) Hasle and non-toxic P. pungens (Grunow) Hasle isolated from Jinhae Bay, Korea. Algae16: 275–285. Search in Google Scholar

Churro, C.I., C.C. Carreira, F.J. Rodrigues, S.C. Craveiro, A.J. Calado, G. Casteleyn and N. Lundholm. 2009. Diversity and abundance of potentially toxic Pseudo-nitzschia Peragallo in Aveiro coastal lagoon, Portugal and description of a new variety, P. pungens var. aveirensis var. nov. Diatom. Res.24: 35–62. Search in Google Scholar

Clarke, K.R. and R.M. Warwick. 2001.Change in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth. pp. 176. Search in Google Scholar

Cusack, C.K., S.S. Bates, M.A. Quilliam, J.W. Patching and R. Raine. 2002. Confirmation of domoic acid production by Pseudo-nitschia australis (Bacillariophyceae) isolated from Irish waters. J. Phycol.38: 1106–1112. Search in Google Scholar

Cusack, C., R. Raine and J.W. Patching. 2004. Occurrence of species from the genus Pseudo-nitzschia Peragallo in Irish waters. Biol. Environ. Proc. Royal Irish Acad.104: 55–74. Search in Google Scholar

Fehling, J. 2004. Diversity, ecology and domoic acid production of Pseudo-nitzschia spp. in Scottish waters. PhD thesis, The Open University, Milton Keynes. pp. 363. Search in Google Scholar

Ferrario, M., E. Sar and S. Sala. 2002. Diatomeas potencialmente toxígenas del 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 Oceanografia, Pontevedra. pp. 169–194. (In Spanish) Search in Google Scholar

Ferrario, M., S. Licea, C.F. Balestrini and G. Ferreyra. 2004. Species of Pseudo-nitzschia in the Drake Passage (54°–61°S to 46°–64°W). In: (K.A. Steidinger, J.H. Landsberg, C.R. Tomas and G.A. Vargo, eds) Harmful algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, St. Pete Beach. pp. 434–436. Search in Google Scholar

Fire, S.E., Z. Wang, M. Berman, G.W. Langlois, S.L. Morton, E. Sekula-Wood and C.R. Benitez-Nelson. 2010. Trophic transfer of the harmful algal toxin domoic acid as a cause of death in a minke whale (Balaenoptera acutorostrata) stranding in Southern California. Aquat. Mamm.36: 342–350. Search in Google Scholar

Fryxell, G.A., M.E. Reap and D.L. Valenic. 1990. Nitzschia pungens Grunow f. multiseries Hasle: observations of a known neurotoxic diatom. Nova Hedwigia, Beih.100: 171–188. Search in Google Scholar

Galicia, M.A. 1987. Modelación hidrodinámica numérica de las bahías de Manzanillo y Santiago. MS thesis, Universidad Nacional Autónoma de México, México. pp. 66. Search in Google Scholar

Galicia, M. and J.H. Gaviño. 1996. Estudio numérico de refracción de oleaje y circulación de la bahía de Manzanillo. GEOS16: 256. Search in Google Scholar

García-Mendoza, E., D. Rivas, A. Olivos-Ortiz, A. Almazán-Becerril, C. Castañeda-Vega and J.L. Peña-Manjarrez. 2009. A toxic Pseudo-nitzschia bloom in Todos Santos Bay, northwestern Baja California, Mexico. Harmful Algae 8: 493–503. Search in Google Scholar

Garrison, D.L., S.M. Conrad, P.P. Eilers and E.M. Waldron. 1992. Confirmation of domoic acid production by Pseudonitzschia australis (Bachillariophyceae) cultures. J. Phycol.28: 604–607. Search in Google Scholar

Grasshoff, K., M. Erhardt, K. Kremling. 1983. Methods of seawater analysis. Second Edition, Verlag Chemie, Weinheim. pp. 600. Search in Google Scholar

Guillard, R.R.L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: (W.L. Smith and M.H. Chanley, eds) Culture of marine invertebrate animals. Springer, New York. pp. 29–60. Search in Google Scholar

Hallegraeff, G.M. 1994. Species of the diatom genus Pseudonitzschia in Australian waters. Bot. Mar.37: 397–412. Search in Google Scholar

Hallegraeff, G.M., C.J.S. Bolch, D.R.A. Hill, I. Jameson, J.-M. LeRoi, A. McMinn, S. Murray, M.F. de Salas and K. Saunders. 2010. Algae of Australia: phytoplankton of temperate coastal waters. Australian Biological Resources Study, Canberra & Commonwealth Scientific and Industrial Research Organisation Publishing, Melbourne. pp. 421. Search in Google Scholar

Hasle, G.R. 1964. Nitzschia and Fragilariopsis species studied in the light and electron microscopes. I. Some marine species of the group Nitzschiella and Lanceolatae. Skr. Norske Vidensk.-Akad. I. Mat.-Nat. Kl. N.S.16: 1–48. Search in Google Scholar

Hasle, G.R. 1965. Nitzschia and Fragilariopsis species studied in the light and electron microscopes. II. The group Pseudonitzschia. Skr. Norske Vidensk.-Akad. I. Mat.-Nat. Kl. N.S.18: 1–45. Search in Google Scholar

Hasle, G.R. 1972. The distribution of Nitzschia seriata Cleve and allied species. Nova Hedwigia, Beih.39: 171–190. Search in Google Scholar

Hasle, G.R. 1993. Nomenclatural notes on marine planktonic diatoms. The family Bacillariaceae. Nova Hedwigia, Beih. 106: 315–321. Search in Google Scholar

Hasle, G.R. 2002. Are most of the domoic acid-producing species of the diatom genus Pseudo-nitzschia cosmopolites? Harmful Algae 1: 137–146. Search in Google Scholar

Hasle, G.R. and E.E. Syvertsen. 1997. Marine diatoms. In: (C.R. Tomas, ed) Identifying marine phytoplankton. Academic Press, San Diego. pp. 5–385. Search in Google Scholar

Hasle, G.R. and N. Lundholm. 2005. Pseudo-nitzschia seriata f. obtusa (Bacillariophyceae) raised in rank based on morphological, phylogenetic and distributional data. Phycologia44: 608–619. Search in Google Scholar

Hasle, G.R., C.B. Lange and E.E. Syvertsen. 1996. A review of Pseudo-nitzschia, with special reference to the Skagerrak, North Atlantic, and adjacent waters. Helgol. Meeresunters.50: 131–175. Search in Google Scholar

Hernández-Becerril, D.U. 1987. Un caso de marea roja en el Golfo de California. Rev. Latinoam. Microbiol.29: 171–177. Search in Google Scholar

Hernández-Becerril, D.U. 1998. Species of the planktonic diatom genus Pseudo-nitzschia of the Pacific coasts of Mexico. Hydrobiologia379: 77–84. Search in Google Scholar

Holtermann, K.E., S.S. Bates, V.L. Trainer, A. Odell and E.V. Armbrust. 2010. Mass sexual reproduction in the toxigenic diatoms Pseudo-nitzschia australis and P. pungens (Bacillariophyceae) on the Washington coast, USA. J. Phycol.46: 41–52. Search in Google Scholar

Hoppenrath, M., M. Elbrächter and G. Drebes. 2009. Marine phytoplankton. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart. pp. 264. Search in Google Scholar

Hostyeva, V., W. Eikrem, B. Edvardsen and G.R. Hasle 2010. Annual cycle of Pseudo-nitzschia species in outer Oslofjorden, Norway. In: (P. Pagou and G. Hallegraeff, eds) Proceedings of the Fourteenth International Conference on Harmful Algae. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Commission of UNESCO, Hersonissos-Crete. p. 38. Search in Google Scholar

Jeffery, B., T. Barlow, K. Moizer, S. Paul and C. Boyle. 2004. Amnesic shellfish poison. Food Chem. Toxicol.42: 545–557. Search in Google Scholar

Kaczmarska, I., M.M. LeGresley, J.L. Martin and J. Ehrman. 2005. Diversity of the diatom genus Pseudo-nitzschia Peragallo in the Quoddy Region of the Bay of Fundy, Canada. Harmful Algae4: 1–19. Search in Google Scholar

Lapworth, C., G.M. Hallegraeffr and P.A. Ajani. 2001. Identification of domoic-acid-producing Pseudo-nitzschia species in Australian waters. In: (G.M. Hallegraeff, S.I. Blackburn, C.J. Bolch and R.J. Lewis, eds) Harmful algae blooms 2000. Intergovernmental Oceanographic Commission of UNESCO, Hobart. pp. 38–41. Search in Google Scholar

Licea, S.S., S. Gómez-Aguirre and J.L. Moreno. 2000. The occurrence of the diatom genus Pseudo-nitzschia Peragallo in Mexican coastal waters, 1979–2000. Proceedings of the Sixteenth International Diatom Symposium. University of Athens, Athens. p. 78. Search in Google Scholar

Lim, H.-C., C.-P. Leaw, S.N.-P. Su, S.-T. Teng, G. Usup, N. Mohammad-Noor, N. Lundholm, Y. Kotaki and P.-T. Lim. 2012. Morpholgy and molecular characterization of Pseudo-nitzschia (Bacillariophyceae) from Malaysian Borneo, including the new species Pseudo-nitzschia circumpora sp. nov. J. Phycol.48: 1232–1247. Search in Google Scholar

Loureiro, S., A. Newton and J.D. Icely. 2005. Microplankton composition, production and upwelling dynamics in Sagres (SW Portugal) during the summer of 2001. Sci. Mar.69: 323–341. Search in Google Scholar

Lundholm, N. and Ø. Moestrup. 2002. The marine diatom Pseudo-nitzschia galaxiae sp. nov. (Bacillariophyceae): morphology and phylogenetic relationships. Phycologia41: 594–605. Search in Google Scholar

Lundholm, N., G.R. Hasle, G.A. Fryxell and P.E. Hargraves. 2002. Morphology, phylogeny and taxonomy of species within the Pseudo-nitzschia americana complex (Bacillariophyceae) with descriptions of two new species, Pseudo-nitzschia brasiliana and Pseudo-nitzschia linea. Phycologia41: 480–497. Search in Google Scholar

Lundholm, N., Ø. Moestrup, G.R. Hasle and K. Hoef-Emden. 2003. A study of the Pseudo-nitzschia pseudodelicatissima/cuspidata complex (Bacillariophyceae): what is P. pseudodelicatissima? J. Phycol.39: 797–813. Search in Google Scholar

Lundholm, N., P.J. Hansen and Y. Kotaki. 2005. Lack of allelopathic effects of the domoic acid-producing marine diatom Pseudo-nitzschia multiseries. Mar. Ecol. Prog. Ser.288: 21–33. Search in Google Scholar

Lundholm, N., Ø. Moestrup, Y. Kotaki, K. Hoef-Emden and C. Scholin. 2006. Inter- and intraspecific variation of the Pseudo-nitzschia delicatissima complex (Bacillariophyceae) illustrated by rRNA probes, morphological data and phylogenetic analyses. J. Phycol.42: 464–481. Search in Google Scholar

Lundholm, N., S.S. Bates, K.A. Baugh, B.D. Bill, L.B. Connell, C. Léger and V.L. Trainer. 2012. Cryptic and pseudo-cryptic diversity in diatoms – with descriptions of Pseudo-nitzschia hasleana sp. nov. and P. fryxelliana sp. nov. J. Phycol.48: 436–454. Search in Google Scholar

Marić, D., Z. Ljubešić, J. Godrijan, D. Viličić, I. Ujević and R. Precali. 2011. Blooms of the potentially toxic diatom Pseudo-nitzschia calliantha Lundholm, Moestrup & Hasle in coastal waters of the northern Adriatic Sea (Croatia). Estuar. Coast. Shelf Sci.92: 323–331. Search in Google Scholar

Moestrup, Ø., R. Akselman, G. Cronberg, M. Elbrächter, S. Fraga, Y. Halim, G. Hansen, M. Hoppenrath, J. Larsen, N. Lundholm, L.N. Nguyen and A. Zingone. 2009. IOC-UNESCO taxonomic reference list of harmful micro algae. Available online at http://www.marinespecies.org/HAB [Accessed 27 March 2013]. Search in Google Scholar

Moita, M.T. 2001. Estrutura, variabilidade e dinâmica do fitoplânton na Costa de Portugal Continental. PhD thesis, University of Lisbon, Lisbon. pp. 272. Search in Google Scholar

Mos, L. 2001. Domoic acid: a fascinating marine toxin. Environ. Toxicol. Phar.9: 79–85. Search in Google Scholar

Moschandreou, K.K. and G. Nikolaidis. 2010. The genus Pseudo-nitzschia (Bacillariophyceae) in Greek coastal waters. Bot. Mar.53: 159–172. Search in Google Scholar

Ochoa, J.L. 2003. ENSO phenomenon and toxic red tides in Mexico. Geofis. Int.42: 505–515. Search in Google Scholar

Orive, E., A. Laza-Martinez, S. Seoane and A. Alonso. 2010. Diversity of Pseudo-nitzschia in the southeastern Bay of Biscay. Diatom Res. 25: 125–145. Search in Google Scholar

Orlova, T.Y. and O.G. Shevchenko. 2002. The first finding of Pseudo-nitzschia americana (Bacillariophyta) in Russian seas. Russ. J. Mar. Biol.28: 336–339. Search in Google Scholar

Orlova, T.Y., I.V. Stonik, N.A. Aizdaicher, S.S. Bates, C. Léger and J. Fehling. 2008. Toxicity, morphology and distribution of Pseudo-nitzschia calliantha, P. multistriata and P. multiseries (Bacillariophyta) from the northwestern Sea of Japan. Bot. Mar.51: 297–306. Search in Google Scholar

Orsini, L., D. Sarno, G. Procaccini, R. Poletti, J. Dahlmann and M. Montresor. 2002. Toxic Pseudo-nitzschia multistriata (Bacillariophyceae) from the Gulf of Naples: morphology, toxin analysis and phylogenetic relationships with other Pseudo-nitzschia species. Eur. J. Phycol.37: 247–257. Search in Google Scholar

Parsons, M.L., Y.B. Okolodkov and J.A. Aké-Castillo. 2012. Diversity and morphology of the species of Pseudonitzschia (Bacillariophyta) of the National Park Sistema Arrecifal Veracruzano, SW Gulf of Mexico. Acta Bot. Mex.98: 51–72. Search in Google Scholar

Priisholm, K., Ø. Moestrup and N. Lundholm. 2002. Taxonomic notes on the marine diatom genus Pseudo-nitzschia in the Andaman Sea near the Island of Phuket, Thailand, with a description of Pseudo-nitzschia micropora sp. nov. Diatom Res.17: 153–175. Search in Google Scholar

Qi, Y., J. Wang and L. Zheng. 1994. The taxonomy and bloom ecology of Pseudo-nitzschia on the coasts of China. In: (A. Nontji, S. Soemodihardjo, A.G. Ilahude, D. Setiapermana, D.P. Preseno, M.K. Moosa and O.T.R. Ongkosongo, eds) IOC-WESTPAC Third International Scientific Symposium. Indonesian Institute of Science, Bali. pp. 88–95. Search in Google Scholar

Quijano-Scheggia, S., E. Garcés, N. Sampedro, K. van Lenning, E. Flo, K. Andree, J.M. Fortuño and J. Camp. 2008. Identification and characterisation of the dominant Pseudo-nitzschia species (Bacillariophyceae) along the NE Spanish coast (Catalonia, NW Mediterranean). Sci. Mar.72: 343–359. Search in Google Scholar

Quijano-Scheggia, S., E. Garcés, N. Lundholm, Ø. Moestrup, K. Andree and J. Camp. 2009. Morphology, physiology, molecular phylogeny and sexual compatibility of the cryptic Pseudo-nitzschia delicatissima complex (Bacillariophyta), including the description of P. arenysensis sp. nov. Phycologia48: 492–509. Search in Google Scholar

Quijano-Scheggia, S., E. Garcés, K.B. Andree, P. de la Iglesia, J. Diogène, J.M. Fortuño and J. Camp. 2010a. Pseudo-nitzschia species on the Catalan coast: characterization and contribution to the current knowledge of the distribution of this genus in the Mediterranean Sea. Sci. Mar.74: 395–410. Search in Google Scholar

Quijano-Scheggia, S., M. Rivera-Vilarelle, E. Garcés, A. Olivos-Ortiz, J.H. Gaviño-Rodríguez, K. Zepeda-Borja, M.A. Galicia-Pérez and M. Patiño-Barragán. 2010b. Seasonal diversity of Pseudo-nitzschia spp. in the central zone of the Mexican Tropical Pacific, Manzanillo, Colima. In: (K. Pagou and G. Hallegraeff, eds) Fourteenth International Conference on Harmful Algae. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Commission of UNESCO, Hersonisson-Crete. p. 49. Search in Google Scholar

Quijano-Scheggia, S., A. Olivos-Ortiz, J.H. Gaviño-Rodríguez, F. Castro-Ochoa, M. Rivera-Vilarelle, M. Galicia-Pérez and M. Patiño-Barragan. 2011. First report of Pseudo-nitzschia brasiliana and P. micropora (Bacillariophycea) found in Cuyutlan Lagoon, Mexico. Rev. Biol. Mar. Oceanog.46: 189–197. Search in Google Scholar

Rhodes, L.L., D. White, M. Syhre and M. Atkinson 1996. Pseudonitzschia species isolated from New Zealand coastal waters: domoic acid production in vitro and links with shellfish toxicity. In: (T. Yasumoto, Y. Oshima and Y. Fukuyo, eds) Harmful and toxic algal blooms. Intergovernmental Oceanographic Commission of UNESCO, Sendai. pp. 155–158. Search in Google Scholar

Rhodes, L., C. Scholin and I. Garthwaite. 1998. Pseudo-nitzschia in New Zealand and the role of DNA probes and immunoassays in refining marine biotoxin monitoring programmes. Nat. Toxins6: 105–111. Search in Google Scholar

Rhodes, L.L., J. Adamson and C. Scholin. 2000. Pseudo-nitzschia multistriata (Bacillariophyceae) in New Zealand. N.Z. J. Mar. Fresh. 34: 463–467. Search in Google Scholar

Rivera, P. 1985. Las especies del género Nitzschia Hassall, sección Pseudonitzschia (Bacillariophyceae), en las aguas marinas chilenas. Gayana Bot.42: 9–38. Search in Google Scholar

Sahraoui, I., S.S. Bates, D. Bouchouicha, H.H. Mabrouk and A.S. Hlaili. 2011. Toxicity of Pseudo-nitzschia populations from Bizerte Lagoon, Tunisia, southwest Mediterranean, and first report of domoic acid production by P. brasiliana. Diatom Res.26: 293–303. Search in Google Scholar

Santiago-Morales, I.S. and E. García-Mendoza. 2011. Growth and domoic acid content of Pseudo-nitzschia australis isolated from northwestern Baja California, Mexico, cultured under batch conditions at different temperatures and two Si:NO3 ratios. Harmful Algae12: 82–94. Search in Google Scholar

Scholin, C.A., F. Gulland, G.J. Doucette, S. Benson, M. Busman, F.P. Chavez, J. Cordaro, R. DeLong, A. De Vogelaere, J. Harvey, M. Haulena, K. Lefebvre, T. Lipscomb, S. Loscutoff, L.J. Lowenstine, R. Marin Iii, P.E. Miller, W.A. McLellan, P.D.R. Moeller, C.L. Powell, T. Rowles, P. Silvagni, M. Silver, T. Spraker, V. Trainer and F.M. Van Dolah. 2000. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature403: 80–84. Search in Google Scholar

Secretaría de Marina. 1973. Estudio geográfico de la región de Manzanillo, Colima. Secretaría de Marina, México, D.F. pp. 157. (In Spanish) Search in Google Scholar

Skov, J., N. Lundholm, Ø. Moestrup and J. Larsen. 1999. Potentially toxic phytoplankton 4. The diatom genus Pseudo-nitzschia (Diatomophyceae/Bacillariophyceae). In: (J.A. Lindley, ed) ICES identification leaflets for plankton. International Council for the Exploration of the Sea, Copenhagen. pp. 1–23. Search in Google Scholar

Smith, J.C., R. Cormier, J. Worms, C.J. Bird and M.A. Quilliam 1990. Toxic blooms of the domoic acid containing diatom Nitzschia pungens in the Cardigan River, Prince Edward Island, in 1988. In: (E. Graneli, B. Sundstrom, L. Edler and D.M. Anderson, eds.) Toxic Marine Phytoplankton. Elsevier, New York, pp. 227–232. Search in Google Scholar

Smith, J.C., K. Pauley, P. Cormier, R. Angus, P. Odense, D. O’Neil, M.A. Quilliam and J. Worms. 1991. Population dynamics and toxicity of various species of Dinophysis and Nitzschia from the southern Gulf of St. Lawrence. Can. Tech. Rep. Fish. Aquat. Sci. 1799: 25. Search in Google Scholar

Solórzano, L. 1969. Determination of ammonia in natural waters by the phenol hypochlorite method. Limnol. Oceanogr.14: 799–801. Search in Google Scholar

Stehr, C.M., L. Connell, K.A. Baugh, B.D. Bill, N.G. Adams and V.L. Trainer. 2002. Morphological, toxicological, and genetic differences among Pseudo-nitzschia (Bacillariophyceae) species in inland embayment’s and outer coastal waters of Washington State, USA. J. Phycol.38: 55–65. Search in Google Scholar

Stonik, I.V., T. Yu. Orlova and N. Lundholm. 2011. Diversity of Pseudo-nitzschia H. Peragallo from the western North Pacific. Diatom Res.26: 121–134. Search in Google Scholar

Strickland, J.D.H. and T.R. Parsons. 1972. A practical handbook of sea water analysis. Fisheries Research Board of Canada, Ottawa. pp. 310. Search in Google Scholar

Takano, H. 1993. Marine diatom Nitzschia multistriata sp. nov. common an inlets of Southern Japan. Diatom8: 39–41. Search in Google Scholar

Terenko, L. and G. Terenko. 2012. Dominant Pseudo-nitzschia (Bacillariophyta) species in the Black Sea (Ukraine). Bot. Lith.18: 27–34. Search in Google Scholar

Thessen, A.E. 2007. Taxonomy and ecophysiology of Pseudo-nitzschia in the Chesapeake Bay. PhD thesis, University of Maryland, Maryland. pp. 231. Search in Google Scholar

Thessen, A.E. and D. Stoecker. 2008. Distribution, abundance and domoic acid analysis of the toxic diatom genus Pseudo-nitzschia from the Chesapeake Bay. Estuar. Coast.31: 664–672. Search in Google Scholar

Throndsen, J. 1995. Estimating cell numbers. In: (G.M. Hallegraeff, D.M. Anderson and A.D. Cembella, eds) Manual on harmful marine microalgae. IOC Manual and Guides UNESCO, Paris. pp. 63–80. Search in Google Scholar

Throndsen, J., G.R. Hasle and K. Tangen. 2007. Phytoplankton of Norwegian coastal waters. Almater Forlag AS, Oslo. pp. 343. Search in Google Scholar

Trainer, V.L. and B.D. Bill. 2004. Characterization of a domoic acid binding site from Pacific razor clam. Aquat. Toxicol.69: 125–132. Search in Google Scholar

Trainer, V.L., N.G. Adams, B.D. Bill, B.F. Anulacion and J.C. Wekell. 1998. Concentration and dispersal of a Pseudo-nitzschia bloom in Penn Cove, Washington, USA. Nat. Toxins6: 113–125. Search in Google Scholar

Trainer, V.L., N.G. Adams, B.D. Bill, C.M. Stehr, J.C. Wekell, P. Moeller, M. Busman and D. Woodruff. 2000. Domoic acid production near California coastal upwelling zones, June 1998. Limnol. Oceanogr.45: 1818–1833. Search in Google Scholar

Trainer, V.L., B.M. Hickey and R.A. Horner. 2002. Biological and physical dynamics of domoic acid production of the Washington coast. 47: 1438–1446. Search in Google Scholar

Trainer, V.L., B.M. Hickey and S.S. Bates. 2008. Toxic diatoms. In: (P.J. Walsh, L.S. Smith., L.E. Fleming, H. Solo-Gabriele and W.H. Gerwick, eds) Oceans and human health: risks and remedies from the sea. Elsevier Science Publishers, New York. pp. 219–237. Search in Google Scholar

Trainer, V.L., B.M. Hickey, E.J. Lessard, W.P. Cochlan, C.G. Trick, M.L. Wells, A. MacFadyen and S.K. Moore. 2009. Variability of Pseudo-nitzschia and domoic acid in the Juan de Fuca eddy region and its adjacent shelves. Limnol. Oceanogr. 54: 289–308. Search in Google Scholar

Trainer, V.L., S.S. Bates, N. Lundholm, A.E. Thessen, W.P. Cochlan, N.G. Adams and C.G. Trick. 2012. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystem health. Harmful Algae14: 271–300. Search in Google Scholar

Utermöhl, H. 1931. Neue Wege in der quantitativen Erfassung des Planktons (Mit besondere Berücksichtigung des Ultraplanktons). Verh. Int. Verein. Theor. Angew. Limnol.5: 267–595. Search in Google Scholar

Villac, M.C. and D.R. Tenenbaum. 2004. The phytoplankton of Guanabara Bay, Brazil: I. historical account of its biodiversity. Biota Neotrop.10: 271–293. Search in Google Scholar

Villac, M.C., G.A. Fryxell, F.P. Chavez and K.R. Buck. 1993. Pseudonitzschia australis Frenguelli and other toxic diatoms from the west coast of the U.S.A.: Distribution and domoic acid production. J. Shellfish Res. 12: 143–143. Search in Google Scholar

Villac, M.C., S. Melo, M.A. Menezes and D.R. Tenebaum. 2005. Pseudo-nitzschia brasiliana (Bacillariophyceae), and opportunistic diatom on the coast of the state or Rio de Janeiro, Brazil. Atlântica, Rio Grande27: 139–145. Search in Google Scholar

Received: 2012-7-6
Accepted: 2013-6-4
Published Online: 2013-07-05
Published in Print: 2013-08-01

©2013 by Walter de Gruyter Berlin Boston