The intricacies of dinoflagellate pellicle cysts: The example of Alexandrium minutum cysts from a bloom-recurrent area (Bay of Baiona, NW Spain)

Deep-Sea Research Part II: Topical Studies in Oceanography

Volumn 57, Issue 3-4, 2010, Pages 166-174

  Bravo, Isabel ^a   Isabel Figueroa, Rosa ^b   Garcés, Esther ^b   Fraga, Santiago ^a   Massanet, Ana ^a  

^a Instituto Español de Oceanografía   (Spain)

^b INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

Alexandrium minutum; Ecdysal cysts; Galician r as; Pellicle cysts; Spain; Temporary cysts

Indexed keywords

ALEXANDRIUM MINUTUM; DINOFLAGELLATE CYSTS; DOUBLE-WALLED; NW SPAIN; TEMPORAL DISTRIBUTION; THIN-WALLED; THREE-TERM; VEGETATIVE CELLS;

BLOOMS (METAL); SAILING VESSELS; THIN WALLED STRUCTURES;

TUMORS;

ALGAL BLOOM; DEVELOPMENTAL BIOLOGY; DINOFLAGELLATE CYST; DORMANCY; FUNCTIONAL MORPHOLOGY; GERMINATION; LIFE CYCLE; POPULATION DENSITY; SPATIAL DISTRIBUTION;

ALEXANDRIUM MINUTUM; DINOPHYCEAE;

EID: 77249119173     PISSN: 09670645     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dsr2.2009.09.003     Document Type: Article

References (94)

1. Alldredge A.L., Passow U., and Haddock S.H.D. The characteristics and transparent exopolymer particle (TEP) content of marine snow formed from thecate dinoflagellates. Journal of Plankton Research 20 (1998) 393-406
2. Anderson D.M., and Wall B. Potential importance of benthic cysts of Gonyaulax tamarensis and Gonyaulax excavata in initiating toxic dinoflagellate blooms. Journal of Phycology 14 (1978) 224-234
3. Anderson D.M. Effects of temperature conditioning on development and germination of Gonyaulax tamarensis (Dinophyceae) hypnozygotes. Journal of Phycology 16 (1980) 166-172
4. Anderson D.M., and Keafer B.A. An endogenous annual clock in the toxic marine dinoflagellate Gonyaulax tamarensis. Nature 325 (1987) 616-617
5. Anderson D.M., Fukuyo Y., and Matsuoka K. Cyst methodologies. In: Hallegraeff G.M., Anderson D.M., and Cembella A.D. (Eds). Manual on Harmful Marine Microalgae (1995), UNESCO, Paris 229-249
6. Anderson D.M. Physiology and bloom dynamics of toxic Alexandrium species, with emphasis on life cycle transitions. In: Anderson D.M., Cembella A.D., and Hallegraeff G.M. (Eds). Physiological Ecology of Harmful Algal Blooms (1998), Springer-Verlag, Berlin, Heidelberg 29-47
7. Balech E. The Genus Alexandrium Halim (Dinoflagellata) (1995), Sherkin Island Marine Station, Sherkin Island, Co. Cork, Ireland
8. Barlow S.B., and Triemer R.E. Alternate life history stages in Amphidinium klebsii (Dinophyceae, Pyrrophyta). Phycologia 27 (1988) 413-420
9. Bolli L., Llaveria G., Garcés E., Guadayol O., van Lenning K., Peters F., and Berdalet E. Modulation of ecdysal cyst and toxin dynamics of two Alexandrium (Dinophyceae) species under small-scale turbulence. Biogeosciences 4 4 (2007) 559-567
10. Behrmann G., and Hardeland R. Ultrastructural characterization of asexual cysts of Gonyaulax polyedra Stein (Dinoflagellata). Protoplasma 185 (1995) 22-27
11. Blackburn S.I., Hallegraeff G.M., and Bolch C.J. Vegetative reproduction and sexual life cycle of the toxic dinoflagellate Gymnodinium catenatum from Tasmania, Australia. Journal of Phycology 25 (1989) 577-590
12. Bolch C.J., Blackburn S.I., Cannon J.A., and Hallegraeff G.M. The resting cyst of the red-tide dinoflagellate Alexandrium minutum (Dinophyceae). Phycologia 30 2 (1991) 215-219
13. Braarud T., and Rossavik H. Observations on the marine dinoflagellate Prorocentrum micans in culture. Avhandingar ugitt av det Norske Videnskaps-Akademii Oslo. Matematisk naturvidenskapelig klasse 1 (1951) 3-18
14. Bravo, I., Fraga S., Figueroa R.I., Pazos Y., Massanet A., Ramilo I., 2010. Bloom dynamics and life cycle strategies of two toxic dinoflagellates in a coastal upwelling system (NW Iberian Peninsula). Deep-Sea Research II 57 (3-4), 222-234
15. Bricheux G., Mahoney D.G., and Gibbs S.P. Development of the pellicle and thecal plates following ecdysis in the dinoflagellate Glenodinium foliaceum. Protoplasma 168 (1992) 159-171
16. Brown E.M. On Oodinium ocellatum Brown, a parasitic dinoflagellate causing epidemic disease in marine fish. Proceedings of the Zoological Society of London 3 (1934) 583-607
17. Buchanan R.J. Studies at Oyster Bay in Jamaica, West Indies, IV. Observations on the morphology and asexual cycle of Pyrodinium bahamense Plate. Journal of Phycology 4 (1968) 271-277
18. Burkholder J.M., and Glasgow H.B. The life cycle and toxicity of Pfiesteria piscicida revisited. Journal of Phycology 38 (2002) 1261-1267
19. Chapman D.V., Dodge J.D., and Heaney S.I. Cyst formation in the freshwater dinoflagellate Ceratium hirundinella (Dinophyceae). Journal of Phycology 18 (1982) 121-129
20. Dale B. Cysts of the toxic red-tide dinoflagellate Gonyaulax excavata (Braarud) Balech from Oslofjorden, Norway. Sarsia 63 (1977) 29-34
21. Dale B. Dinoflagellate resting cysts: "benthic plankton". In: Fryxell G.A. (Ed). Survival Strategies of the Algae (1983), Cambrige University Press 69-136
22. Delgado M. A new "diablillo parasite" in the toxic dinoflagellate Alexandrium catenella as a possibility to control harmful algal blooms. Harmful Algae News 19 (1999) 1-3
23. Doucette G.J., Cembella A.D., and Boyer G.L. Cyst formation in the red tide dinoflagellate Alexandrium tamarense (Dinophyceae): effects of iron stress. Journal of Phycology 25 (1989) 721-731
24. Drebes G., and Schnepf E. Paulsenella Chatton (Dinophyta), ectoparasites of marine diatoms: development and taxonomy. Helgoland. Meeresunt 42 (1988) 563-581
25. Elbrächter M., and Drebes G. Life cycles, phylogeny and taxonomy of Dissodinium and Pyrocystis (Dinophyta). Helgoländer wiss Meeresunters 31 (1978) 347-366
26. Faust M.A. Prorocentrum belizeanum, Prorocentrum elegans, and Prorocentrum caribbaeum, three new benthic species (Dinophyceae) from a mangrove island, Twin Cays, Belize. Journal of Phycology 29 (1993) 100-107
27. Faust M.A. Morphology and life cycle events Pyrophacus steinii (Schiller) Wall et Dale (Dinophyceae). Journal of Phycology 34 (1998) 173-179
28. Figueroa R.I., and Bravo I. Sexual reproduccion and two different encystment strategies of Lingulodinium polyedrum (Dinophyceae) in culture. Journal of Phycology 41 (2005) 370-379
29. Figueroa R.I., Bravo I., and Garcés E. Effects of nutritional factors and different parental crosses on the encystment and excystment of Alexandrium catenella (Dinophyceae) in culture. Phycologia 44 6 (2005) 658-670
30. Figueroa R.I., Bravo I., and Garcés E. Multiple routes of sexuality in Alexandrium taylori (Dinophyceae) in culture. Journal of Phycology 42 5 (2006) 1028-1039
31. Figueroa R.I., Bravo I., Garcés E., and Ramilo I. Nuclear features and nutrient effect on Gymnodinium catenatum (Dinophyceae) sexual stages. Journal of Phycology 42 (2006) 67-77
32. Figueroa R.I., Garcés E., and Bravo I. Comparative study of the life cycles of Alexandrium tamutum and Alexandrium minutum (Gonyaulacales, Dinophyceae) in culture. Journal of Phycology 43 (2007) 1039-1053
33. Figueroa R.I., Bravo I., Ramilo I., Pazos Y., and Angeles M. New life-cycle stages of Gymnodinium catenatum (Dinophyceae): laboratory and field observations. Aquatic Microbial Ecology 52 (2008) 13-23
34. Figueroa R.I., Bravo I., and Garcés E. The life cycle of Alexandrium peruvianum (Dinophyceae) in culture. Harmful Algae 7 (2008) 653-663
35. Fistarol G.O., Legrand C., Rengefors K., and Granéli E. Temporary cyst formation in phytoplankton: a response to allelopathic competitors?. Environmental Microbiology 6 8 (2004) 791-798
36. Fraga F. Upwelling off the Galician coast, Northwest Spain. In: Richard F.A. (Ed). Coastal Upwelling (1981), American Geophysical Union, Washington, DC 176-182
37. Fritz L., and Triemer R.E. A rapid simple technique utilizing Calcofluor White M2r for the visualization of dinoflagellate thecal plates. Journal of Phycology 21 (1985) 662-664
38. Fritz L., Anderson D.M., and Triemer R.E. Ultrastructural aspects of sexual reproduction in the red tide dinoflagellate Gonyaulax tamarensis. Journal of Phycology 25 (1989) 95-107
39. Garcés E., Delgado M., Masó M., and Camp J. Life history and in situ growth rates of Alexandrium taylori (Dinophyceae, Pyrrophyta). Journal of Phycology 34 (1998) 880-887
40. Garcés E., Masó M., and Camp J. A recurrent and localized dinoflagellate bloom in a Mediterranean beach. Journal of Plankton Research 21 (1999) 2373-2391
41. Garcés E., Maso M., and Camp J. Role of temporary cysts in the population dynamics of Alexandrium taylori (Dinophyceae). Journal of Plankton Research 24 (2002) 681-686
42. Garcés E., Bravo I., Vila M., Figueroa R.I., Masó M., and Sampedro N. Relationship between vegetative cells and cyst production during Alexandrium minutum bloom in Arenys de Mar harbour (NW Mediterranean). Journal of Plankton Research 26 6 (2004) 637-645
43. Giacobbe M.G., and Yang X. The life history of Alexandrium taylori (Dinophyceae). Journal of Phycology 35 2 (1999) 331-338
44. Gribble K.E., Anderson D.M., and Coats D.W. Sexual and Asexual Processes in Protoperidinium steidingerae Balech (Dinophyceae), with Observations on Life-Hystory Stages of Protoperidinium depressum (Bailey) Balech (Dinophyceae). Journal of Eukaryotic Microbiology 56 1 (2009) 88-103
45. Grzebyk D., and Berland B. Influences of temperature, salinity and irradiance on growth of Prorocentrum minimum (Dinophyceae) from the Mediterranean Sea. Journal of Plankton Research 18 (1996) 1837-1849
46. Hardeland R. Induction of cyst formation by low temperature in the dinoflagellate Gonyaulax polyedra Stein - dependence on circadian phase and requirement of light. Experientia 50 (1994) 60-62
47. Horiguchi T., and Chihara M. Life-cycle, behavior and morphology of a new tide pool dinoflagellate, Gymnodinium pyrenoidosum sp-nov (Gymnodiniales, Pyrrophyta). Botanical Magazine-Tokyo 101 (1988) 255-265
48. Imada N., Honjo T., Shibata H., Oshima Y., Nagai K., Matsuyama Y., and Uchida T. The quantities of Heterocapsa circularisquama cells transferred with shellfish consignments and the possibility of its establishment in new areas. In: Hallegraeff G.M., Bolch C.J., and Lewis R.J. (Eds). Harmful Algal Blooms (2000), UNESCO, Paris 474-476
49. Jensen M.O., and Moestrup O. Autecology of the toxic dinoflagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. European Journal of Phycology 32 (1997) 9-18
50. Juhl A.R., and Latz M.I. Mechanisms of fluid shear-induced inhibition of population growth in a red-tide dinoflagellate. Journal of Phycology 38 (2002) 683-694
51. Kibler, S.R., 1999. Encystment, excystment and photosynthetic activity in the temporary cysts of Amphidinium carterae. Ph.D. Thesis. Old Dominion University, Norfolk, Virginia, 75pp.
52. Kim C.H., Cho H.J., Shin J.B., Moon C.H., and Matsuoka K. Regeneration from hyaline cysts of Cochlodinium polykrikoides (Gymnodiniales, Dinophyceae), a red tide organism along the Korean coast. Phycologia 41 6 (2002) 667-669
53. Kim C.J., Kim H.G., Kim C.H., and Oh H.M. Life cycle of the ichthyotoxic dinoflagellate Cochlodinium polykrikoides in Korean coastal waters. Harmful Algae 1 6 (2007) 104-111
54. Kita T., Fukuyo Y., Tokuda H., and Hirano R. Life history and ecology of Goniodoma pseudogoniaulax (Pyrrophyta) in a rockpool. Bulletin of Marine Science 37 2 (1985) 643-651
55. Kita T., Fukuyo Y., Tokuda H., and Hirano R. Sexual reproduction of Alexandrium hiranoi (Dinophyceae). Bulletin of Plankton Society of Japan 39 2 (1993) 79-85
56. Kremp A., and Parrow M.W. Evidence for asexual resting cysts in the life cycle of the marine peridinoid dinoflagellate, Scrippsiella hangoei. Journal of Phycology 42 2 (2006) 400-409
57. Laabir M., Amzil Z., Lassus P., Masseret E., Tapilatu Y., De Vargas R., and Grzebyk D. Viability, growth and toxicity of Alexandrium catenella and Alexandrium minutum (Dinophyceae) following ingestion and gut passage in the oyster Crassostrea gigas. Aquatic Living Resources 20 1 (2007) 51-57
58. Laabir M., and Gentien P. Survival of toxic dinoflagellates after gut passage in the Pacific oyster Crassostrea gigas Thunburg. Journal of Shellfish Research 18 1 (1999) 217-222
59. Lavin A., Díaz del Río G., Cabanas J.M., and Casas G. Afloramiento en el Noroeste de la Península Ibérica. Índices de afloramiento para el punto 43°N 11°W. Informes Técnicos del Instituto Español de Oceanografía 91 (1991) 1-39
60. Litaker R.W., Vandersea M.W., Kibler S.R., Madden V.J., Noga E.J., and Tester P.A. Life cycle of the heterotrophic dinoflagellate Pfiesteria piscicida (Dinophyceae). Journal of Phycology 38 (2002) 442-463
61. Manjares B., and Fritz L. Temporary cysts cycles in the freshwater dinoflagellates Peridinium volzii and Peridinium inconspicuum. Proceedings of XVI International Botanical Congress, Journal of Phycology (1999) 22
62. Marasovic I. Encystment and Excystment of Gonyaulax polyedra during a red tide. Estuarine, Coastal and Shelf Science 28 (1989) 35-41
63. Matrai P., Thompson B., and Keller M. Circannual excystment of resting cysts of Alexandrium spp. from eastern Gulf of Maine populations. Deep-Sea Research II 52 19-21 (2005) 2522-2542
64. Mayali X., Franks P.J.S., and Azam F. Bacterial induction of temporary cyst formation by the dinoflagellate Lingulodinium polyedrum. Aquatic Microbial Ecology 50 (2007) 51-62
65. Montresor M. The life history of Alexandrium pseudogonyaulax (Gonyaulacales, Dinophyceae). Phycologia 34 6 (1995) 444-448
66. Murray S., and Patterson D.J. The benthic dinoflagellate genus Amphidinium in south-eastern Australian waters, including three new species. European Journal of Phycology 37 2 (2002) 279-298
67. Nagasaki K., Yamaguchi M., and Imai I. Algicidal activity of a killer bacterium against the harmful red tide dinoflagellate Heterocapsa circularisquama isolated from Ago Bay. Japan. Nippon-Suisan-Gakkaish 66 (2000) 666-673
68. Olli K. Temporary cyst formation of Heterocapsa triquetra (Dinophyceae) in natural populations. Marine Biology 145 (2004) 1-8
69. Østergaard M., and Moestrup O. Autecology of the toxic dinoflagellate Alexandrium ostenfeldii: life history and growth at different temperatures and salinities. European Journal of Phycology 32 (1997) 9-18
70. Parrow M.W., and Burkholder J.M. Reproduction and sexuality in Pfiesteria shumwayae (Dinophyceae). Journal of Phycology 39 (2003) 697-711
71. Pfiester L.A. Sexual reproduction of Peridinium willei (Dinophyceae). Journal of Phycology 12 (1976) 234-238
72. Pfiester L.A., and Skvarla J.J. Heterothallism and thecal development in the sexual life history of Peridinium volzii (Dinophyceae). Phycologia 18 1 (1979) 13-18
73. Pfiester L., and Lynch R.A. Amoeboid stages and sexual reproduction of Cystodinium bataviense and its similarity do Dinococcus (Dinophyceae). Phycologia 19 3 (1980) 178-183
74. Pfiester L.A. Dinoflagellate sexuality. International Review of Cytology 114 (1989) 249-272
75. Rengefors K., and Anderson D.M. Environmental and endogenous regulation of cyst germination in two freshwater dinoflagellates. Journal of Phycology 34 (1998) 568-577
76. Rintala J.M., Spilling K., and Blomster J. Temporary cyst enables long-term dark survival of Scrippsiella hangoei (Dinophyceae). Marine Biology 152 (2007) 57-62
77. Sakamoto B., Hokama Y., Horgen F.D., Scheuer P.J., Kan Y., and Nagai H. Isolation of a sulfoquinovosyl monoacyglycerol from Bryopsis sp. (Chlorophyta): identification of a factor causing a possible species-specific ecdysis response in Gambierdiscus toxicus (Dinophyceae). Journal of Phycology 36 (2000) 924-931
78. Sampayo M.A. Encystment and excystment of a Portuguese isolate culture of Amphidinium carterae in culture. In: Anderson M.A., White M., and Baden L. (Eds). Toxic Dinoflagellates (1985), Elsevier, New York 125-130
79. Scarrat A.M., Scarrat D.J., and Scarrat M.G. Survival of live Alexandrium tamarense cells in mussel an scallop spat under simulated transfer conditions. Journal of Shellfish Research 12 (1993) 383-388
80. Schmitter R.E. Temporary cysts of Gonyaulax excavata: effects of temperature and light. In: Taylor D.L., and Seliger H.H. (Eds). Toxic Dinoflagellate Blooms (1979), Elsevier North Holland Inc., New York 123
81. Seo K.S., and Fritz L. Cell-wall morphology correlates with vertical migration in the non-motile marine dinoflagellate Pyrocystis noctiluca. Marine Biology 137 (2000) 589-594
82. Seo K.S., and Fritz L. Ultrastructure of vegetative cysts of Pyrocystis (Dinophyta), with special reference to PAS bodies and trichocysts. Phycologia 41 1 (2002) 10-14
83. Skerratt J.H., Bowman J.P., Hallegraeff G., James S., and Nichols P.D. Algicidal bacteria associated with blooms of a toxic dinoflagellate in a temperate Australian estuary. Marine Ecology Progress Series 244 (2002) 1-15
84. Spero H.J., and Moree M.D. Phagotrophic feeding and its importance to the life-cycle of the holozoic dinoflagellate, Gymnodinium fungiforme. Journal of Phycology 17 (1981) 43-51
85. Springer J.J., Shumway S.E., Burkholder J.M., and Glasgow H.B. Interactions between the toxic estuarine dinoflagellate Pfiesteria piscicida and two species of bivalve molluscs. Marine Ecology Progress Series 245 (2002) 1-10
86. Tarutani K., Nagasaki K., Itakura S., and Yamaguchi M. Isolation of a virus infecting the novel shellfish-killing dinoflagellate Heterocapsa circularisquama. Aquatic Microbial Ecology 23 (2001) 103-111
87. Taylor F.J.R. A description of the benthic dinoflagellate associated with maitotoxin and ciguatoxin, including observations on Hawaiian material. In: Taylor D.L., and Seliger H.H. (Eds). Toxic dinoflagellate blooms (1979), Elsevier, North-Holland 71-76
88. Taylor F.J.R. On dinoflagellate evolution. BioSystems 13 (1980) 65-108
89. Toth G.B., Norén F., Selander E., and Pavia H. Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals. Proceedings of the Royal Society of London B: Biological Sciences 271 (2004) 733-738
90. Uchida T., Matsuyama Y., Yamaguchi M., and Honjo T. Growth interatctions between a red tide Heterocapsa circularisquama and some other phytoplankton species in culture. In: Yasumoto T., Oshima Y., and Fukuyo Y. (Eds). Harmful and Toxic Aldal Blooms (1996), UNESCO, Paris 369-372
91. Uchida T., Toda S., Matsuyama Y., Yamaguchi M., Kotani Y., and Honjo T. Interactions between the red tide dinoflagellates Heterocapsa circularisquama and Gymnodinium mikimotoi in laboratory culture. Journal of Experimental Marine Biology and Ecology 241 (1999) 285-299
92. Ucko M., Elbrächter M., and Schnepf E. A Crypthecodinium cohnii-like dinoflagellate feeding myzocytotically on the unicellular red alga Porphyridium sp. European Journal of Phycology 32 (1997) 133-140
93. 2+ in stimulated bioluminescence of the dinoflagellate Lingulodinium polyedrum. Journal of Experimental Biology 205 (2002) 2971-2986
94. von Stosch H.A. Observations on vegetative reproduction and sexual life cycles of two freshwater dinoflagellates Gymnodinium pseudopalustre Schiller and Woloszynskia apiculata sp. nov. British Phycological Journal 8 (1973) 105-134