Influence of temperature, salinity and irradiance on the growth and cell yield of the harmful red tide dinoflagellate Alexandrium catenella colonizing Mediterranean waters

Journal of Plankton Research

Volumn 33, Issue 10, 2011, Pages 1550-1563

  Laabir, Mohamed ^a   Jauzein, Cecile ^b   Genovesi, Benjamin ^c   Masseret, Estelle ^a   Grzebyk, Daniel ^a   Cecchi, Philippe ^d   Vaquer, André ^a   Perrin, Yvon ^a   Collos, Yves ^a  

^a CNRS   (France)

^b UNIVERSITY OF TEXAS   (United States)

^c INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^d INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

Alexandrium catenella; cell yield; growth; irradiance; salinity; temperature; Thau lagoon; toxic blooms

Indexed keywords

ALGAL BLOOM; DINOFLAGELLATE; ECOPHYSIOLOGY; ESTUARINE ECOSYSTEM; GROWTH RATE; IRRADIANCE; PHYSICOCHEMICAL PROPERTY; SEA SURFACE SALINITY; SEA SURFACE TEMPERATURE; SEASONAL VARIATION;

ETANG DE THAU; FRANCE; HERAULT; LANGUEDOC-ROUSSILLON; MEDITERRANEAN SEA; MEDITERRANEAN SEA (WEST);

ALEXANDRIUM CATENELLA; DINOPHYCEAE;

EID: 80052567294     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbr050     Document Type: Article

References (73)

1. Abadie, E., Amzil, Z., Belin, C. et al. (1999) Contamination de l'étang de Thau par Alexandrium tamarense. Episode de novembre à décembre 1998. Ifremer, 44 pp. Available online at http://www.ifremer.fr/ docelec/doc/1999/rapport-884.pdf (accessed on 10 April 2009).
2. Adachi, M., Sako, Y. and Ishida, Y. (1996) Analyses of Alexandrium (Dinophyceae) species using sequences of the 5.8S ribosomal DNA and internal transcribed spacer regions. J. Phycol., 32, 424-432. (Pubitemid 26270240)
3. Andersen, V. and Nival, P. (1988) A pelagic ecosystem model simulating production and sedimentation of biogenic particles: role of salps and copepods. Mar. Ecol. Prog. Ser., 44, 37-50.
4. Anderson, D. M., Kulis, D. M. and Binder, B. J. (1984) Sexuality and cyst formation in the dinoflagellate Gonyaulax tamarensis: cyst yield in batch cultures. J. Phycol., 20, 418-425.
5. Baek, S. H., Shimode, S. and Kikuchi, T. (2008) Growth of dinoflagel-lates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: The role of temperature, light intensity and photoperiod. Harmful Algae, 7, 163-173. (Pubitemid 350235335)
6. Band-Schmidt, C. J., Morquecho, L., Lechuga-Deveze, C. H. et al. (2004) Effects of growth medium, temperature, salinity and seawater source on the growth of Gymnodinium catenatum (Dinophyceae) from Bah́ia Concepción, Gulf of California, Mexico. J. Plankton. Res., 26, 1459-1470. (Pubitemid 40084310)
7. Bec, B., Husseini-Ratrema, J., Collos, Y. et al. (2005) Phytoplankton seasonal dynamics in a Mediterranean coastal lagoon: emphasis on the picoeucaryote community. J. Plankton Res., 27, 881-894. (Pubitemid 41567075)
8. Bravo, I., Vila, M., Maso, M. et al. (2008) Alexandrium catenella and Alexandrium minutum blooms in the Mediterranean Sea: toward the identification of ecological niches. Harmful Algae, 7, 515-522.
9. Burkholder, J. M., Glibert, P. M. and Skelton, H. M. (2008) Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae, 8, 77-93.
10. Carignan, M. O., Montoya, N. G. and Carreto, J. I. (2002) Long-term effects of ultraviolet radiation on the composition of pigment and mycosporine-like amino acids (MAAs) composition in Alexandrium catenella. In Arzul, G. editor. Aquaculture, Environment and Marine Phytoplankton. Vol. 34. 2002. p. 191-207. Ed. IFREMER. Actes Colloq. Proceedings of a Symposium held in Brest, 21-23 May 2001.
11. Cembella, A. D., (1998) Ecophysiology and metabolism of paralytic shellfish toxins in marine microalgae. In Anderson, D. M., Cembella, A. D. and Hallegraeff, G. M. (eds), Physiological Ecology of Harmful Blooms. Vol. G41. NATO ASI Series, Berlin, pp. 381-403.
12. Chen, H. and Jiang, J-G. (2009) Osmotic responses of Dunaliella to the changes of salinity. J. Cellular. Physiol., 129, 251-258.
13. Collos, Y., Bec, B., Jauzein, C. et al. (2009) Oligotrophication and emergence of picocyanobacteria and a toxic dinoflagellate in Thau lagoon, southern France. J. Sea Research., 61, 68-75.
14. Collos, Y., Gagne, C., Laabir, M. et al. (2004) Nitrogenous nutrition of Alexandrium catenella (Dinophyceae) in cultures and in Thau lagoon, southern France. J. Phycol., 40, 96-103. (Pubitemid 38241642)
15. Collos, Y., Vaquer, A., Laabir, M. et al. (2007) Contribution of several nitrogen sources to growth of Alexandrium catenella during blooms in Thau lagoon, Southern France. Harmful Algae, 6, 781-789. (Pubitemid 47575967)
16. Cordova, J. L. and Muller, I. (2002) Use of PCR and partial sequencing of the large-subunit rRNA gene to indentify Alexandrium catenella (Dinophycea) from the South of Chile. Harmful Algae, 1, 343-350. (Pubitemid 37379153)
17. Doucette, G. L., McGovern, E. R. and Babinchak, A. J. (1999) Algicidal bacteria active against Gymnodinium breve (Dinophyceae). I. Bacterial isolation and characterization of killing activity. J. Phycol., 35, 1447-1454.
18. Etheridge, S. M. and Roesler, C. (2005) Effects of temperature, irradiance, and salinity on photosynthesis, growth rates, total tox-icity, and toxin composition for Alexandrium fundyense isolates from the Gulf of Maine and Bay of Fundy. Deep-Sea Research II., 52, 2491-2500. (Pubitemid 41659358)
19. Falkowski, P. G., Owens, T. G., Ley, A. C. et al. (1981) Effects of growth irradiance levels on the ratio of reaction centers in two species of marine phytoplankton. Plant Physiol., 68, 969-973.
20. Falkowski, P. G. and Raven, J. A. (1997) Aquatic photosynthesis. Blackwell Science, Malden, MA.
21. 2 and temperature effects on sympatric Heterosigma akashiwo and Prorocentrum minimum. Harmful Algae, 7, 76-90. (Pubitemid 350088633)
22. Fulco, V. K. and Gayoso, A. M. (2004) Effects of light, temperature and salinity on the growth rate of Alexandrium tamarense from Patagonia (Argentina). In Steidinger, K. A., Landsberg, J. H., Tomas, C. R. and Vargo, G. A. (eds), Harmful Algae 2002. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography, and Intergovernmental Oceanographic Commission of UNESCO, pp. 391-392.
23. Garcès, E., Masó, M. and Camp, J. (1999) A recurrent and localized dinoflagellate bloom in a Mediterranean beach. J. Plankton. Res., 21, 2373-2391. (Pubitemid 30018157)
24. Garcés, E., Vila, M., Maso, M. et al. (2005) Taxon-specific analysis of growth and mortality rates of harmful dinoflagellates during bloom conditions. Mar. Ecol. Prog. Ser., 301, 67-79. (Pubitemid 41608875)
25. Genovesi, B., Laabir, M., Masseret, E. et al. (2009) Dormancy and germination features in resting cysts of Alexandrium tamarense species complex (Dinophyceae) can facilitate bloom formation in a shallow lagoon (Thau, southern France). J. Plankton. Res., 31, 1209-1224.
26. Genovesi, B., Shin-Grzebyk, M-S., Grzebyk, D. et al. (2011) Assessment of cryptic species diversity within blooms and cyst bank of the Alexandrium tamarense complex (Dinophyceae) in a Mediterranean lagoon facilitated by semi-multiplex PCR. J. Plankton. Res., 33, 405-414.
27. Giacobbe, M. G., Oliva, F. D. and Maimone, G. (1996) Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum, a PSP potential producer, in a Mediterranean lagoon. Estuar. Coastal Shelf Sci., 42, 539-549.
28. Glibert, P. M., Anderson, D. M., Gentien, P. et al. (2005) The global complex phenomena of harmful algal blooms. Oceanography, 18, 130-141.
29. Grzebyk, D., Bechemin, C., Ward, C. et al. (2003) Effects of salinity and two coastal waters on the growth and toxin content of the dino-flagellate Alexandrium minutum. J. Plankton. Res., 25, 1185-1199. (Pubitemid 37284081)
30. Grzebyk, D. and Berland, B. (1996) Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. J. Plankton. Res., 18, 1837-1849.
31. Guillard, R. L. R. (1973) Division rates. In Stein, J. R. (ed.), Handbook of Phycological Methods. Cultures Methods and Growth Measurements. Cambridge University Press, Cambridge, pp. 290-311.
32. Hallegraeff, G. M. (1993) A review of harmful algal blooms and their apparent global increase. Phycologia., 32, 79-99. (Pubitemid 24410302)
33. Hamasaki, K., Horie, M., Tokimitsu, S. et al. (2001) Variability in tox-icity of the dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, Western Japan, as a reflection of changing environmental conditions. J. Plankton. Res., 23, 271-278. (Pubitemid 32418029)
34. Harrison, P. J., Waters, R. E. and Taylor, F.J. R. (1980) A broad spectrum artificial seawater medium for coastal and open ocean phyto-plankton. J. Phycol., 16, 28-35.
35. Hwang, D. F. and Lu, Y. H. (2000) Influence of environmental and nutritional factors on growth, toxicity, and toxin profile of dinofla-gellate Alexandrium minutum. Toxicon, 38, 1491-1503. (Pubitemid 30206995)
36. Ichimi, K., Yamasaki, M., Okumura, Y. et al. (2001) The growth and cyst formation of a toxic dinoflagellate, Alexandrium tamarense, at low water temperatures in northeastern Japan. J. Exp. Mar. Biol. Ecol., 261, 17-29. (Pubitemid 33649573)
37. Ignatiades, L., Gotsis-Skretas, O. and Metaxatos, A. (2007) Field and culture studies on the ecophysiology of the toxic dinoflagellate Alexandrium minutum (Halim) present in Greek coastal waters. Harmful Algae, 6, 153-165. (Pubitemid 46157016)
38. Iwasaki, J. (1992) Effect of temperature, salinity and pH on the growth of Alexandrium catenella, a paralytic shellfish poison producing dinofla-gellate Bull. Fish. Exp. Stn. Ibaraki-Ken., 30, 93-100.
39. Jauzein, C., Labry, C., Youenou, A. et al. (2010) Growth and phosphorus uptake by the toxic dinoflagellate Alexandrium catenella (Dinophyceae) in response to phosphate limitation. J. Phycol., 46, 926-936.
40. Jensen, M. O. and Moestrup, O. (1997) Autoecology of the toxic dino-flagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. Eur. J. Phycol., 32, 9-18.
41. Kim, D. I., Matsuyama, Y., Nagasoe, S. et al. (2004) Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykrikoides Margalef (Dinophyceae). J. Plankton. Res., 26, 61-66. (Pubitemid 38119178)
42. Kudela, R. M., Seeyave, S. and Cochlan, W. P. (2010) The role of nutrients in regulation and promotion of harmful algal blooms in upwelling systems. Prog. Oceanogr., 85, 122-135.
43. Laanaia, N., Vaquer, A., Fiandrino, A. et al. (2008) Wind and temperature controls on the occurrence of blooms of Alexandrium in Thau Lagoon (Western Mediterranean). In The 13th International Conference on Harmful Algae, Hong Kong, 3-7 November 2008, Program and Abstracts, p. 142.
44. Leong, S. C. Y., Maekawa, M. and Taguchi, S. (2010) Carbon and nitrogen acquisition by the toxic dinoflagellate Alexandrium tamarense in response to different nitrogen sources and supply modes. Harmful Algae, 9, 48-58.
45. Lilly, E. L., Halanych, K. M. and Anderson, D. M. (2007) Species boundaries and global biogeography of the Alexandrium tamarense complex (Dinophyceae). J. Phycol., 43, 1329-1338. (Pubitemid 350221965)
46. Lilly, E. L., Kulis, D. M., Gentien, P. et al. (2002) Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from western Pacific: evidence from DNA and toxin analysis. J. Plankton. Res., 24, 443-452. (Pubitemid 34589573)
47. Lim, P. T. and Ogata, T. (2005) Salinity effect on growth and toxin production of four tropical Alexandrium species (Dinophyceae). Toxicon, 45, 699-710. (Pubitemid 40432595)
48. MacKenzie, L., De Salas, M., Adamson, J. et al. (2004) The dinofla-gellate genus Alexandrium (Halim) in New Zealand coastal waters: comparative morphology, toxicity and molecular genetics. Harmful Algae, 3, 71-92. (Pubitemid 38105885)
49. Matsuda, A., Nishijima, T., Fukami, K. et al. (2006) Growth kinetics and paralytic shellfish poisoning toxin production in phosphorus-limited cultures of Alexandrium catenella. Nippon Suisan Gakkaishi., 72, 193-200. (Pubitemid 43806377)
50. Mayfield, A. B. and Gates, R. D. (2007) Osmoregulation in anthozoan-dinoflagellate symbiosis. Comp. Biochem. Physiol., 147, 1-10. (Pubitemid 46467461)
51. Mazouni, N., Deslous-Paoli, J. M. and Landrein, S. (1998) Influence d'un élevage ostréicole sur les flux de nutriments et d'oxygène dans un écosystème lagunaire. Oceanologica Acta., 21, 845-858. (Pubitemid 29032439)
52. Nagasoe, S., Kim, D., Shimasaki, Y. et al. (2006) Effects of temperature, salinity and irradiance on the growth of the red tide dinofla-gellate Gyrodinium instriatum Freudenthal et Lee. Harmful Algae, 5, 20-25. (Pubitemid 41814795)
53. Navarro, J. M., Munoz, M. G. and Contreras, A. M. (2006) Temperature as a factor regulating growth and toxin content in the dinoflagellate Alexandrium catenella. Harmful Algae, 5, 762-769. (Pubitemid 44666564)
54. Neveux, J. and Lantoine, F. (1993) Spectrofluorimetric assay of chlorophylls and phaeopigments using the least squares approximation technique. Deep Sea Res., 40, 1747-1765. (Pubitemid 24430062)
55. Nguyen-Ngoc, L. (2004) An autoecological study of the potentially toxic dinoflagellate Alexandrium affine isolated from Vietnamese waters. Harmful Algae, 3, 117-129. (Pubitemid 38215117)
56. Parkhill, J. P. and Cembella, D. L. (1999) Effects of salinity, light and inorganic nitrogen on growth and toxigenicity of the marine dino-flagellate Alexandrium tamarense from northeastern Canada. J. Plankton Res., 21, 939-955.
57. Penna, A., Garcés, E., Vila, M. et al. (2005) Alexandrium catenella (Dinophycea), a toxic ribotype expanding in the NW Mediterranean sea. Mar Biol., 148, 13-23. (Pubitemid 41605627)
58. Plus, M., Chapelle, A., Ménesguen, A. et al. (2003) Modelling seasonal dynamics of biomasses and nitrogen contents in a seagrass meadow (Zostera noltii Hornem.): application to the Thau lagoon (French Mediterranean coast). Ecol. Modell., 16, 213-238. (Pubitemid 36280548)
59. Scholin, C. A. and Anderson, D. M. (1994) Identification of group and strain-specific genetic markers for globally distributed Alexandrium (Dinophycea). I RFLP analysis of SSUrRNA genes. J. Phycol., 30, 744-754. (Pubitemid 2139691)
60. Siu, G. K. Y., Young, M. L. C. and Chan, D. K. O. (1997) Environmental and nutritional factors which regulate population dynamics and toxin production in the dinoflagellate Alexandrium cate-nella. Hydrobiologia, 352, 117-140.
61. Smayda, T. J. (1990) Novel and nuisance phytoplankton blooms in the sea: evidence for a global epidemic. In Graneli, E., Sundström, B., Edler, L. and Anderson, D.M. (eds), Toxic Phytoplankton. Elsevier, New York, pp. 29-40.
62. Smayda, T. J. (2008) Complexity in the eutrophication-harmful algal bloom relationship, with comment on the importance of grazing. Harmful Algae, 8, 140-151.
63. Suttle, C. A. (1994) The significance of viruses to mortality in aquatic communities. Microb. Ecol., 28, 237-243.
64. Thébault, J. M. (1985) Etude expérimentale de la nutrition d'un copépode commun (Temora stylifera Dana), effets de la température et de la concentration de nourriture. J. Exp. Mar. Biol. Ecol., 93, 223-234.
65. Tian, R. C. (2006) Toward standard parameterizations in marine biological modeling. Ecol. Modell., 193, 363-386. (Pubitemid 43247804)
66. Turner, J. T. and Tester, P. A. (1997) Toxic marine phytoplankton, zoo-plankton grazers, and pelagic food webs. Limnol. Oceangr., 42, 1203-1214.
67. Varela, D. E. and Harrison, P. J. (1999) Effect of ammonium on nitrate utilization by Emiliania huxleyi, a coccolithophore from the oceanic northeastern Pacific. Mar. Ecol. Prog. Ser., 186, 67-74. (Pubitemid 29498755)
68. Vila, M., Garces, E., Maso, M. et al. (2001) Is the distribution of the toxic dinoflagellate Alexandrium catenella expanding along the NW Mediterranean coast? Mar. Ecol. Prog. Ser., 23, 497-514.
69. Vila, M., Giaccobbe, M. G., Maso, M. et al. (2005) A comparative study on recurrent blooms of Alexandrium minutum in two Mediterranean coastal areas. Harmful Algae, 4, 673-695. (Pubitemid 40328619)
70. Wang, D. Z. and Hsieh, P. H. (2005) Growth and toxin production in batch cultures of a marine dinoflagellate Alexandrium tamarense HK9301 isolated from the South China Sea. Harmful Algae, 4, 401-410.
71. Xu, N., Duan, S., Li, A. et al. (2010) Effects of temperature, salinity and irradiance on the growth of harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful Algae, 9, 13-17.
72. Yamaguchi, M. and Honjo, T. (1989) Effect of temperature, salinity and irradiance on the growth of the noxious red tide flagellate Gymnodinium nagasakiense (Dinophyceae). Nippon Suisan Gakkaishi., 55, 2029-2036.
73. Yeung, P. K. K., Wong, F. T. W. and Wong, J. T. Y. (2002) Large subunit rDNA sequences from Alexandrium catenevilalla strains isolated during algal blooms in Hong Kong. J. Appl. Phycol., 14, 147-150. (Pubitemid 34536171)