Comparative study of the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture

Journal of Phycology

Volumn 43, Issue 5, 2007, Pages 1039-1053

  Figueroa, Rosa Isabel ^a   Garcés, Esther ^b   Bravo, Isabel ^a  

^a INSTITUTO ESPAÑOL DE OCEANOGRAFÍA   (Spain)

^b IRTA   (Spain)

Author keywords

Alexandrium minutum; Alexandrium tamutum; Cysts; Dinoflagellates; Encystment; Excystment; Flow cytometry; Nitrogen; Phosphorus; Sexual reproduction

Indexed keywords

ALEXANDRIUM; ALEXANDRIUM MINUTUM; ALEXANDRIUM TAMUTUM; DINOPHYCEAE; GONYAULACALES;

EID: 34250219453     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2007.00393.x     Document Type: Article

References (60)

1. Anderson, D. M., Chisholm, S. W. Watras, C. J. 1983. The importance of life cycle events in the population dynamics of Gonyaulax tamarensis. Mar. Biol. 76:179 83.
2. Anderson, D. M. Keafer, B. A. 1987. An endogenous annual clock in the toxic marine dinoflagellate Gonyaulax tamarensis. Nature 325:616 7.
3. Anderson, D. M., Kulis, D. M., Doucette, G. J., Gallagher, J. C. Balech, E. 1994. Biogeography of toxic dinoflagellates in the genus Alexandrium from the northeastern United States and Canada. Mar. Biol. 120:467 78.
4. Balech, E. 1995. The Genus Alexandrium Halim (Dinoflagellata). Sherkin Island Marine Station Publication, Sherkin Island, Co. Cork, Ireland, pp. 151.
5. Bhaud, Y., Soyer-Gobillard, M. O. Salmon, J. M. 1988. Transmission of gametic nuclei through a fertilization tube during mating in a primitive dinoflagellate, Prorocentrum micans Ehr. J. Cell Sci. 89:197 206.
6. Blackburn, S. I., Bolch, C. J. S., Haskard, K. A. Hallegraeff, G. M. 2001. Reproductive compatibility among four global populations of the toxic dinoflagellate Gymnodinium catenatum (Dinophyceae). Phycologia 40:78 87.
7. Blackburn, S. I., Hallegraeff, G. M. Bolch, C. J. 1989. Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum. J. Phycol. 25:577 90.
8. Bolch, C. J., Blackburn, S. I., Cannon, J. A. Hallegraeff, G. M. 1991. The resting cyst of the red-tide dinoflagellate Alexandrium minutum (Dinophyceae). Phycologia 30:215 9.
9. Bolch, C. J. S. Reynolds, M. J. 2002. Species resolution and global distribution of microreticulate dinoflagellate cysts. J. Plankton Res. 24:565 78.
10. Cetta, C. M. Anderson, D. M. 1990. Cell cycle studies of the dinoflagellates Gonyaulax polyedra Stein and Gyrodinium uncatenum Hulburt during asexual and sexual reproduction. J. Exp. Mar. Biol. Ecol. 135:69 84.
11. Delgado, M., Estrada, M., Camp, J., Fernández, J. V., Santmartí, M. Lletí, C. 1990. Development of a toxic Alexandrium minutum Halim (Dinophyceae) bloom in the harbour of Sant Carles de la Rápìta (Ebro-Delta, northwestern Mediterranean). Sci. Mar. 54:1 7.
12. Figueroa, R. I. Bravo, I. 2005a. A study of the sexual reproduction and determination of mating type of Gymnodinium nolleri (Dinophyceae) in culture. J. Phycol. 41:74 83.
13. Figueroa, R. I. Bravo, I. 2005b. Sexual reproduction and two different encystment strategies of Lingulodinium polyedrum (Dinophyceae) in culture. J. Phycol. 41:370 9.
14. Figueroa, R. I., Bravo, I. Garcés, E. 2005. Effects of nutritional factors and different parental crosses on the encystment and excystment of Alexandrium catenella (Dinophyceae) in culture. Phycologia 44:658 70.
15. Figueroa, R. I., Bravo, I. Garcés, E. 2006a. Multiple routes of sexuality in Alexandrium taylori (Dinophyceae) in culture. J. Phycol. 42:1028 39.
16. Figueroa, R. I., Bravo, I., Garcés, E. Ramilo, I. 2006b. Nuclear features and nutrient effect on Gymnodinium catenatum (Dinophyceae) sexual stages. J. Phycol. 42:67 77.
17. Figueroa, R. I., Rengefors, K. Bravo, I. 2006c. Parental effects and meiosis on sexual offspring of Gymnodinium nolleri (Dinophyceae). J. Phycol. 42:350 62.
18. Fritz, L. M., Anderson, D. M. Triemer, R. E. 1989. Ultrastructural aspects of sexual reproduction in the red tide dinoflagellate Gonyaulax tamarensis. J. Phycol. 25:95 107.
19. Fukuyo, Y. 1985. Morphology of Protogonyaulax tamarensis (Lebour) Taylor and Protogonyaulax catenella (Whedon and Kofoid) Taylor from Japanese coastal waters. Bull. Mar. Sci. 37:529 37.
20. Fukuyo, Y., Sako, Y., Matsuoka, K., Imai, I., Takahashi, M. Watanabe, M. 2003. Biological character of red-tide organisms. In Okaichi, T. Ed. Red Tides. Terra Scientific Publishing Company, Tokyo, pp. 61 153.
21. Gallagher, J. C. 1998. Genetic variation in harmful algal bloom species: an evolutionary ecology approach. In Anderson, D. M., Cembella, A. D. Hallegraeff, G. M. Eds. Physiological Ecology of Harmful Algal Blooms. NATO ASI Series. Springer-Verlag, Berlin, pp. 225 42.
22. Garcés, E., Bravo, I., Vila, M., Figueroa, R. I., Masó, M. Sampedro, N. 2004. Relationship between vegetative cells and cyst production during Alexandrium minutum bloom in Arenys de Mar harbour (NW Mediterranean). J. Plankton Res. 26:637 45.
23. Garcés, E., Delgado, M., Masó, M. Camp, J. 1998. Life history and in situ growth rates of Alexandrium taylori (Dinophyceae, Pyrrophyta). J. Phycol. 34:880 7.
24. Gayoso, A. Fulco, V. K. 2006. Occurrence patterns of Alexandrium tamarense (Lebour) Balech populations in the Golfo Nuevo (Patagonia, Argentina), with observations on ventral pore occurrence in natural and cultured cells. Harmful Algae 5:233 41.
25. Giacobbe, M. G., Oliva, F. D. Maimone, G. 1996. Environmental factors and seasonal occurrence of the dinoflagellate Alexandrium minutum, a PSP potential producer, in a Mediterranean Lagoon. Estuar. Coast. Shelf Sci. 42:539 49.
26. Giacobbe, M. G. Yang, X. 1999. The life history of Alexandrium taylori (Dinophyceae). J. Phycol. 35:331 8.
27. Grassholff, K. 1976. Determination of nutrients. In Giesler, G. Sosath, S. Eds. Methods of Seawater Analysis. Verlag Chemie, Weinheim, Germany, pp. 117 78.
28. Gretchen, A. G. Cáceres, C. E. 2003. Genetic versus environmental influence on pigment variation in the ephippia of Daphnia pulicaria. Freshw. Biol. 48:1971 82.
29. Guillard, R. R. L. Hargraves, P. E. 1993. Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32:234 6.
30. Halim, Y. 1960. Alexandrium minutum nov. g. nov. sp. dinoglagellè provocant des 'eaux rouges'. Vie Milieu 11:102 5.
31. Hallegraeff, G. M., Marshall, J. A., Valentine, J. Hardiman, S. 1998. Short cyst-dormancy period of an Australian isolate of the toxic dinoflagellate Alexandrium catenella. Mar. Freshw. Res. 49:415 20.
32. Hallegraeff, G. M., Steffensen, D. A. Wetherbee, R. 1988. Three estuarine Australian dinoflagellates that can produce paralytic shellfish toxins. J. Plankton Res. 10:533 41.
33. Hansen, G., Daugbjerg, N. Franco, J. M. 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 35.
34. Harvey, H. W. 1955. The Chemistry and Fertility of Sea Waters. The University Press, Cambridge, UK, 224 pp.
35. Hayhome, B. A., Whitten, D. H., Harkins, K. R. Pfiester, L. A. 1987. Intraspecific variation in the dinoflagellate Perdinium volzii. J. Phycol. 23:573 80.
36. Honsell, G. 1993. First report of Alexandrium minutum in northern Adriatic waters (Mediterranean Sea). In Smayda, T. J. Shimizu, Y. Eds. Toxic Phytoplankton Blooms in the Sea. Elsevier, Amsterdam, pp. 127 32
37. Honsell, G., Poletti, R., Pompei, M., Sidari, L., Milandri, A., Casadei, C. Viviani, R. 1996. Alexandrium minutum Halim and PSP contamination in the northern Adriatic Sea (Mediterranean Sea). In Yasumoto, T., Oshima, Y. Fukuyo, Y. Eds. Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission, UNESCO, Sendai, Japan, pp. 77 80.
38. Joseph, G. 1879. Über Grotten-Infusioren. Zool. Anz. 2:114 8.
39. Kim, C. H., Cho, H. J., Shin, J. B., Moon, C. H. Matsuoka, K. 2002. Regeneration from hyaline cysts of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae), a red tide organism along the Korean coast. Phycologia 41:667 9.
40. Lilly, E. L., Kulis, D. M., Gentien, P. Anderson, D. M. 2002. Paralytic shellfish poisoning toxins in France linked to a human-introduced strain of Alexandrium catenella from the western Pacific: evidence from DNA and toxin analysis. J. Plankton Res. 24:443 52.
41. MacKenzie, L. Todd, K. 2002. Alexandrium camurascutulum sp. nov. (Dinophyceae): a new dinoflagellate species from New Zealand. Harmful Algae 1:295 300.
42. Margalef, R. 1997. A special role for phosphorus? In Kinne, O. Ed. Our Biosphere Vol. 10. Excellence in Ecology. Ecology Institute, Oldendorf/Luhe, Germany, pp. 140 2.
43. Moestrup, Ø., Codd, G. A., Elbrächter, M., Faust, M. A., Fraga, S., Fukuyo, Y., Cronberg, G., Halim, Y., Taylor, F. J. R. Zingone, A. 2002. IOC Taxonomic Reference List of Toxic Algae. Intergovernmental Oceanographic Commission of UNESCO, Paris. Available at: http://ioc.unesco.org/ hab/data.htm
44. Montresor, M., John, U., Beran, A. Medlin, L. K. 2004. Alexandrium tamutum sp. nov. (Dinophyceae): a new non-toxic species in the genus Alexandrium. J. Phycol. 40:398 11.
45. Murphy, L. S. Guillard, R. R. L. 1976. Biochemical taxonomy of marine phytoplankton by enzyme electrophoresis. I. The centric diatoms Thalassiosira pseudonana Hasle and Heimdal and Thalassiosira fluviatilis Hustedt. J. Phycol. 12:9 13.
46. Nezan, E. Piclet, G. 1991. Ecotoxicological studies of some recent Alexandrium sp. outbreaks in France. In Fremy, J. M. Ed. Actes du Colloque sur les Biotoxines Marines, Paris, 30-31 Janvier 1991 [Proceedings of Symposium on Marine Biotoxins, Paris, 30-31 January 1991]. Editions du Centre National dÉtudes Vetérinaires et Alimentaires, Maisons-Alfort, France, pp. 195 201.
47. Park, H.-D. Hayashi, H. 1993. Role of encystment and excystment of Peridinium bipes f. occulatum (Dinophyceae) in freshwater red tides in Lake Kizaki, Japan. J. Phycol. 29:435 41.
48. Parrow, M. W. Burkholder, J. M. 2003. Estuarine heterotrophic cryptoeridiniopsoids (Dinophyceae): life cycle and culture studies. J. Phycol. 39:678 96.
49. Parrow, M. W. Burkholder, J. M. 2004. The sexual life cycles of Pfiesteria piscicida and cryptoperidiniopsoids (Dinophyceae). J. Phycol. 40:664 73.
50. Parrow, M. W., Burkholder, J. M., Deamer, N. J. Zhang, C. 2002. Vegetative and sexual reproduction in Pfiesteria spp. (Dinophyceae) cultured with algal prey, and inferences for their classification. Harmful Algae 1:5 33.
51. Parsons, K. E. 1997. Contrasting patterns of heritable geographic variation in shell morphology and growth potential in the marine gastropod Bembicium vittatum: evidence from field experiments. Evolution 51:784 96.
52. Pfiester, L. A. Anderson, D. M. 1987. Dinoflagellate reproduction. In Taylor, F. J. R. Ed. The Biology of the Dinoflagellates. Botanical Monographs 21. Blackwell, Oxford, UK, pp. 611 48.
53. Probert, I., Lewis, J. Erard-Le Denn, E. 2002. Morphological details of the life history of Alexandrium minutum (Dinophyceae). Cryptogam. Algol. 23:343 55.
54. Sako, Y., Ishida, Y., Kadota, H. Hata, Y. 1984. Sexual reproduction and cyst formation in the freshwater dinoflagellate Peridinium cunningtonii. Bull. Jpn. Soc. Sci. Fish/Nissuishi 50:743 50.
55. Uchida, T. 1991. Sexual reproduction of Scrippsiella trochoidea isolated from Muroran Harbor Hokkaido. Nippon Suisan Gakkaishi 57:1215.
56. Uchida, T., Matsuyama, Y., Yamaguchi, M. Honjo, T. 1996. The life cycle of Gyrodinium instriatum (Dinophyceae) in culture. Phycol. Res. 44:119 23.
57. Vila, M., Camp, J., Garcés, E., Masó, M. Delgado, M. 2001. High resolution spatio-temporal detection of potentially harmful dinoflagellates in confined waters of the NW Mediterranean. J. Plankton Res. 23:497 514.
58. Von Stosch, H. A. 1972. La signification cytologique de la "cyclose nucléaire" dans le cycle de vie des Dinoflagelle's. Bull. Soc. Bot. Fr. Mem. 1972:201 12
59. Von Stosch, H. A. 1973. Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates Gymnodinium pseudopalustre Schiller and Woloszynkskia apiculata sp. nov. Br. Phycol. J. 8:105 34.
60. Yoshimatsu, S. 1984. Sexual reproduction of Protogonyaulax catenella in culture, 2. Determination of mating type. Bull. Plankton Soc. Jpn. 31:107 11.