Parasites and phytoplankton, with special emphasis on dinoflagellate infections

Journal of Eukaryotic Microbiology

Volumn 51, Issue 2, 2004, Pages 145-155

  Park, Myung Gil ^a   Yih, Wonho ^b   Coats, D Wayne ^c  

^a Chonnam National University   (South Korea)

^b Kunsan National University   (South Korea)

^c SMITHSONIAN ENVIRONMENTAL RESEARCH CENTER   (United States)

Author keywords

Biological control; Dinoflagellate; Harmful algal bloom; Parasite; Parasitism; Phytoplankton; Protist

Indexed keywords

FRESH WATER; SEA WATER;

ALGAL BLOOM; BIOLOGICAL CONTROL; DINOFLAGELLATE; HOST-PARASITE INTERACTION; PHYTOPLANKTON;

ANIMAL; BACTERIAL PHENOMENA AND FUNCTIONS; BIOLOGICAL PEST CONTROL; CONFERENCE PAPER; CYTOLOGY; DINOFLAGELLATE; ECOSYSTEM; FOOD CHAIN; FUNGUS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; PHYTOPLANKTON; POPULATION DYNAMICS;

ANIMALS; BACTERIAL PHYSIOLOGY; DINOFLAGELLIDA; ECOSYSTEM; FOOD CHAIN; FRESH WATER; FUNGI; HOST-PARASITE RELATIONS; PEST CONTROL, BIOLOGICAL; PHYTOPLANKTON; POPULATION DYNAMICS; SEAWATER; WATER MICROBIOLOGY;

ALGAE; AMOEBOPHRYA; ANIMALIA; BACILLARIOPHYTA; BACTERIA (MICROORGANISMS); DINOPHYCEAE; FUNGI; PARVILUCIFERA INFECTANS; PERKINSEA; PROTISTA; PROTOZOA;

EID: 1942505741     PISSN: 10665234     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2004.tb00539.x     Document Type: Conference Paper

References (130)

1. Abeliovich, A. & Dikbuck, S. 1977. Factors affecting infection of Scenedesmus obliquus by a Chytridium sp. in sewage oxidation ponds. Appl. Environ. Microbiol., 6:832-836.
2. Bailey-Watts, A. E. & Lund, J. W. G. 1973. Observations on a diatom bloom in Loch Leven, Scotland. Biol. J. Linn. Soc., 5:235-253.
3. Berland, B. R., Maestrini, S. Y. & Grzebyk, D. 1995. Observations on possible life cycle stages of the dinoflagellates Dinophysis cf. acuminate, Dinophysis acuta and Dinophysis pavillardi. Aquat. Microb. Ecol., 9:183-189.
4. Blinn, D. W. & Button, K. S. 1973. The effect of temperature on parasitism of Pandorina sp. by Dargeatdia mammillata B. Schröder in an Arizona mountain lake. J. Phycol., 9:323-326.
5. Boltovskoy, A. 1984. Ralacion huesped-parasito entre el quiste de Peridinium willei y el oomicete Aphanomycopsis peridiniella n. sp. Limnobios, 2:635-645.
6. Borgert, A. 1898. Beiträge zur Kenntnis in Sticholonche zanclea und Acanthometridenarten vorkommenden Parasiten (Spiralköper Fol, Amoebophrya Köppen). Z. Wiss. Zool. Abstract A, 63:141-186.
7. Bratbak, G., Heldal, M., Norland, S. & Thingstad, T. F. 1990. Viruses as partners in spring bloom microbial trophodynamics. Appl. Environ. Microbiol., 56:1400-1405.
8. Brugerolle, G. 2002. Cryptophagus subtilis: a new parasite of cryptophytes affiliated with the Perkinsozoa lineage. Europ. J. Protistol., 37:379-390.
9. Bruning, K. 1991a. Infection of the diatom Asterionella by a chytrid. I. Effects of light on reproduction and infectivity of the parasite. J. Plankton Res., 13:103-117.
10. Bruning, K. 1991b. Infection of the diatom Asterionella by a chytrid. I. Effects of light on survival and epidemic development of the parasite. J. Plankton Res., 13:119-129.
11. Bruning, K. 1991c. Effects of phosphorus limitation on the epidemiology of a chytrid phytoplankton parasite. Freshwater Biol., 25:409-417.
12. Bruning, K. 1991d. Effect of temperature and light on the population dynamics of the Asterionella-Rhizophydium association. J. Plankton Res., 13:707-719.
13. Bruning, K. & Ringelberg, J. 1987. The influence of phosphorus limitation of the diatom Asterionella formosa on the zoospore production of its fungal parasite Rhizophydium planktonicum. Hydrobiol. Bulletin, 21:49-54.
14. Brussaard, C. P. D. 2004. Viral control of phytoplankton populations - a review. J. Eukaryot. Microbiol., 51:125-138.
15. Bütschli, O. 1883-1887. Protozoa. Abtheilung II. Mastigophora. In: Bronn, H. G. (ed.), Klassen und Ordungen des Thier-Reichs. C. F. Winter, Leipzig. 1:617-1097.
16. Cachon, J. 1964. Contribution à l'étude des péridiniens parasites. Cytologie, cycles évolutifs. Ann. Sci. Nat. Zool., 6:1-158.
17. Cachon, J. & Cachon, M. 1987. Parasitic dinoflagellates. In: Taylor, F. J. R. (ed.), The Biology of Dinoflagellates. Blackwell Sci. Publ., Oxford. p. 571-610.
18. Cachon, J., Cachon, M. & Bouquaheux, F. 1969. Myxodinium pipiens gen. nov., sp. nov., péridinien parasite d'Halosphaera. Phycologia, 8:157-164.
19. Canter, H. M. 1972. A guide to the fungi occurring on planktonic blue-green algae. In: Desikachary, T. V. (ed.), Proceedings of the Symposium on Taxonomy and Biology of Blue-green Algae. Madras, University of Madras. p. 148-158.
20. Canter, H. M. & Heaney, S. I. 1984. Observations on zoosporic fungi of Ceratium spp. in lakes of the English Lake District: Importance for phytoplankton population dynamics. New Phytol., 97:601-612.
21. Canter, H. M. & Jaworski, G. H. M. 1978. The isolation, maintenance, and host-range studies of a chytrid Rhizophydium planktonicum Canter emend., parasitic on Asterionella formosa Hassall. Ann. Bot., 42: 967-979.
22. Canter, H. M. & Jaworski, G. H. M. 1981. The effect of light and darkness upon infection of Asterionella formosa Hassall by the chytrid Rhizophydium planktonicum Canter emend. Ann. Botany, 47:13-30.
23. Canter, H. M. & Jaworski, G. H. M. 1982. Some observations on the alga Fragilaria crotonensis Kitton and its parasitism by two chytridiaceous fungi. Ann. Bot., 49:429-446.
24. Canter, H. M. & Lund, J. W. G. 1948. Studies on plankton parasites. I. Fluctuations in the numbers of Asterionella formosa Hass. in relation to fungal epidemics. New Phytol., 47:238-261.
25. Canter, H. M. & Lund, J. W. G. 1951. Studies on plankton parasites. III. Examples of the interaction between parasitism and other factors determining the growth of diatoms. Ann. Bot., 15:359-371.
26. Canter, H. M. & Lund, J. W. G. 1953. Studies on plankton parasites. II. The parasitism of diatoms with special reference to lakes in the English Lake District. Trans. British Mycol. Soc., 36:13-37.
27. Canter, H. M. & Lund, J. W. G. 1969. The parasitism on planktonic desmids by fungi. Österr. Bot. Z., 116:351-377.
28. Chase, Z. & Price, N. M. 1997. Metabolic consequences of iron deficiency in heterotrophic marine protozoa. Limnol. Oceanogr., 42: 1673-1684.
29. Chatton, É. & Biecheler, B. 1934. Les Coccidinidae, Dinoflagellés coccodiomorphes parasites de Dinoflagellés, et le phylum des Phytodinozoa. C. R. Acad. Sci., Paris, 199:252-255.
30. Chatton, É. & Biecheler, B. 1935. Les Amoebophrya et les Hyalosaccus: leur cycle évolutif. L'ordre nouveau des Coelomastigines dans les Flagellés. C. R. Acad. Sci., Paris, 200:505-507.
31. Chatton, É. & Biecheler, B. 1936. Documents nouveaux relatifs aux Coccidinides (Dinoflagellés parasites). La sexualité du Coccidinium mesnili n. sp. C. R. Acad. Sci., Paris, 203:573-576.
32. Coats, D. W. 1999. Parasitic life styles of marine dinoflagellates. J. Eukaryot. Microbiol., 46:402-409.
33. Coats, D. W. & Bockstahler, K. R. 1994. Occurrence of the parasitic dinoflagellate Amoebophrya ceratii in Chesapeake Bay populations of Gymnodinium sanguineum. J. Eukaryot. Microbiol., 41:586-593.
34. Coats, D. W. & Heisler, J. J. 1989. Spatial and temporal occurrence of the parasitic dinoflagellate Duboscquella cachoni and its tintinnine host, Eutintinnus pectinis, in Chesapeake Bay. Mar. Biol., 101:401-409.
35. Coats, D. W. & Park, M. G. 2002. Parasitism of photosynthetic dinoflagellates by three strains of Amoebophrya (Dinophyta): parasite survival, infectivity, generation time, and host specificity. J. Phycol., 38: 520-528.
36. Coats, D. W., Adam, E. J., Gallegos, C. L. & Hedrick, S. 1996. Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA. Aquat. Microb. Ecol., 11:1-9.
37. Coats, D. W., Bockstahler, K. R., Berg, G. M. & Sniezek, J. H. 1994. Dinoflagellate infections of Favella panamensis from two North American estuaries. Mar. Biol., 119:105-113.
38. Delgado, M. 1999. A new "diablillo parasite" in the toxic dinoflagellate Alexandrium catenella as a possibility to control harmful algal blooms. Harmful Algae News, 19:1-3.
39. Doggett, M. S. & Porter, D. 1995. Further evidence for host-specificity variants in Zygorhizidium planktonicum. Mycologia, 87:161-171.
40. Doucette, G. J., Kodama, M., Franca, S. & Gallacher, S. 1998. Bacterial interactions with harmful algal bloom species: bloom ecology, toxigenesis, and cytology. In: Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algal Blooms. NATO ASI Series G: Ecological Sciences, Vol. 41. Springer-Verlag, Heidelberg. p. 619-47.
41. Drebes, G. & Schnepf, E. 1982. Phagotrophy and development of Paulsenella cf. chaetoceratis (Dinophyta), an ectoparasite of the diatom Streptotheca thamesis. Helgoländer Meeresunters., 35:501-515.
42. Drebes, G. & Schnepf, E. 1988. Paulsenella Chatton (Dinophyta), ectoparasite of marine diatoms: development and taxonomy. Helgoländer Meeresunters., 42:563-581.
43. Elbrächter, M., 1973. Population dynamics of Ceratium in coastal waters of the Kiel Bay. Oikos (Suppl.), 15:43-48.
44. Elbrächter, M. & Schnepf, E. 1998. Parasites of harmful algae. In: Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algal Blooms. NATO ASI Series G: Ecological Sciences, Vol. 41. Springer-Verlag, Heidelberg. p. 351-369.
45. Erard-Le Denn, E., Chrétiennot-Dinet, J.-M. & Probert, I. 2000. First report of parasitism on the toxic dinoflagellates Alexandrium minutum Halim. Estuar. Coast. Shelf Sci., 50:109-113.
46. Falkowski, P. G., Hopkins, T. S. & Walsh, J. J. 1980. An analysis of factors affecting oxygen depletion in the New York Bight. J. Mar. Res. 38:479-506.
47. Ferrier-Pagès, C., Karner, M. & Rassoulzadegan, F. 1998. Release of dissolved amino acids by flagellates and ciliates grazing on bacteria. Oceanol. Acta, 21:485-494.
48. Fiedler, P. C. 1982. Zooplankton avoidance and reduced grazing responses to Gymnodinium splendens (Dinophyceae). Limnol. Oceanogr., 27:961-965.
49. Fogg, G. E., 1983. The ecological significance of extracellular products of phytoplankton photosynthesis. Bot. Mar., 26:3-14.
50. Franca, S. 1976. On the presence of virus-like particles in the dinoflagellate Gyrodinium resplendens (Hulburt). Protistologica, 12:425-430.
51. Fritz, L. & Nass, M. 1992. Development of the endoparasitic dinoflagellate Amoebophrya ceratii within host dinoflagellate species. J. Phycol., 28:312-320.
52. Fuhrman, J., 1992. Bacterioplankton roles in cycling of organic matter: the microbial food web. In: Falkowski, P. G. & Woodhead, D. (ed.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York. p. 361-383.
53. Gárate Lizárraga, I. & Siqueiros-Beltrones, D. A. 2003. Infections of Ceratium furca by the parasitic dinoflagellate Amoebophrya ceratii (Amoebophryidae) in the Mexican Pacific. Acta Bot. Mex., 65:1-9.
54. Gisselson, L. Å., Carlsson, P., Granéli, E. & Pallon, J. 2002. Dinophysis blooms in the deep euphotic zone of the Baltic Sea: do they grow in the dark? Harmful Algae, 1:401-418.
55. Gobler, C. J., Hutchins, D. A., Fisher N. S., Cosper E. M. & Sanudo-Wilhelmy, S. A. 1997. Release and bioavailability of C, N, P, Se, and Fe following viral lysis of a marine chrysophyte. Limnol. Oceanogr., 42:1492-1504.
56. Granéli, E., Olsson, P., Carlsson, P., Granéli, W. & Nylander, C. 1993. Weak 'top-down' control of dinoflagellate growth in the coastal Skagerrak. J. Plank. Res., 15:213-237.
57. Gunderson, J. H., Goss, S. H. & Coats, D. W. 2001. FISH probes for the detection of the parasitic dinoflagellate Amoebophrya sp. infecting the dinoflagellate Akashiwo sanguinea in Chesapeake Bay. J. Eukaryot. Microbiol., 48:670-675.
58. Gunderson, J. H., John, S. A., Boman, W. C., II & Coats, D. W. 2002. Multiple strains of the parasitic dinoflagellate Amoebophrya exist in Chesapeake Bay. J. Eukaryot. Microbiol., 49:469-474.
59. Hansen, P. J., Cembella, A. D. & Moestrup, Ø. 1992. The marine dinoflagellate Alexandrium ostenfeldii: paralytic shellfish toxin concentration, composition, and toxicity to a tintinnid ciliate. J. Plankton Res., 28:597-603.
60. Heaney, S. I., Lund, J. W. G., Canter, H. M. & Gray, K. 1988. Population dynamics of Ceratium spp. in three English lakes, 1945-1985. Hydrobiology, 161:133-148.
61. Holfeld, H. 1998. Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake. New Phytol., 138:507-517.
62. Huntley, M., Sykes, P., Marin, V. & Rohan, S. 1986. Chemically-mediated rejection of dinoflagellate prey by copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence, and significance. Mar. Ecol. Prog. Ser., 28:105-120.
63. Jacobson, D. M. 1987. The ecology and feeding biology of thecate heterotrophic dinoflagellates. Dissertation. Woods Hole Oceanographic Institution-Massachusetts Institute of Technology Joint Program. 210 pp. Available on microfilms from University of Michigan Accession Number 101132.
64. Janson, S. L., Gisselson, P. S., Salomon, P. S. & Granéli, E. 2000. Evidence for multiple species within the endoparasitic dinoflagellate Amoebophrya ceratii as based on 18S rRNA gene-sequence analysis. Parasitol. Res., 86:929-933.
65. Johansson, M. & Coats, D. W. 2002. Ciliate grazing on the parasite Amoebophrya sp. decreases infection of the red-tide dinoflagellate Akashiwo sanguinea. Aquat. Microb. Ecol., 28:69-78.
66. Kim, Y. G., Park, M. G. & Yih, W. H. 2002. Host-parasite system in a red tide dinoflagellate Prorocentrum minimum: (1) Life cycle stages of the parasitic dinoflagellate Amoebophrya sp. The Sea, J. Korean Soc. Oceanogr., 7:221-225.
67. Kirchner, M., Sahling, G., Schütt, C., Döpke, H & Uhlig, G. 1999. Intracellular bacteria in the red tide-forming heterotrophic dinoflagellate Noctiluca scintillans. Arch. Hydrobiol. Spec. Issues Advanc. Limnol., 54:297-310.
68. Koob, D. D. 1966. Parasitism of Asterionella formosa Hass. by a chytrid in two lakes of the Rawah Wild Area of Colorado. J. Phycol., 2:41-45.
69. Koeppen, N. 1894. Amoebophrya stycholonchae nov. gen. et sp. "corps spiral" de Fol. Zool. Anz., 17:417-424.
70. Koeppen, N. 1903. Hyalosaccus ceratii nov. gen., nov. sp., parasit Dinoflagellat'. Zapiski Kiev. Obshch., 16:89-135.
71. Kofoid, C. A. & Swezy, O. 1921. The Free-Living Unarmored Dinoflagellata. Memoirs of the University of California. Vol 5. Univ. California Press, Berkeley.
72. Kudoh, S. & Takahashi, M. 1990. Fungal control of population changes of the planktonic diatom Asterionella formosa in a shallow eutrophic lake. J. Phycol., 26:239-244.
73. Kudoh, S. & Takahashi, M. 1992. An experimental test of host population-size control by fungal parasitism in the planktonic diatom Asterionella formosa using mesocosms in a natural lake. Arch. Hydrobiol., 124:293-307.
74. Küpper, F. C. & Müller, D. G. 1999. Massive occurrence of the heterokont and fungal parasites Anisolpidium, Eurychasma, and Chytridium in Pylaiella littoralis (Ectocarpales, Phaeophyceae). Nov. Hedw., 69:381-389.
75. Lampert, W. 1978. Release of dissolved organic carbon by grazing zooplankton. Limnol. Oceanogr., 23:831-834.
76. Lancelot, C. 1979. Gross excretion rates on natural marine phytoplankton and heterotrophic uptake of excreted products in the southern North Sea, as determined by short-term kinetics. Mar. Ecol. Prog. Ser., 1:179-186.
77. Lebour, M. V. 1917. The Peridiniales of Plymouth Sound from the region beyond the breakwater. J. Mar. Biol. Assoc. U. K., 11:183-200.
78. Lebour, M. V. 1925. The Dinoflagellates of Northern Seas. The Mayflower Press, William Brendon & Son, Ltd., Plymouth.
79. Maranda, L. 2001. Infection of Prorocentrum minimum (Dinophyceae) by the parasite Amoebophrya sp. (Dinoflagellea). J. Phycol., 37:245-248.
80. Masters, M. J. 1971. The ecology of Chytridium deltanum and other fungus parasites on Oocystis spp. Canadian J. Bot., 49:75-87.
81. Müller, D. G., Küpper, F. C. & Küpper, H. 1999. Infection experiments reveal broad host range of Eurychasma dicksoni (Oomycota) and Chytridium polysiphoniae (Chytridiomycota), two eukaryotic parasites in marine brown algae (Phaeophyceae). Phycol. Res., 47:217-223.
82. Nagasaki, K., Tomaru, Y., Tarutani, K., Katanozaka, N., Yamanaka, S., Tanabe, H. & Yamaguchi, M. 2003. Growth characteristics and interspecies host specificity of a large virus infecting the dinoflagellate Heterocapsa circulaisquama. Applied Environ. Microb., 69:2580-2586.
83. Nagata, T. & Kirchman, D. L. 1992. Release of dissolved organic matter by heterotrophic protozoa: implications for microbial food webs. Arch. Hydrobiol. Beih. Ergebn. Limnol., 35:99-109.
84. Nagata, T. 2000. Production mechanisms of dissolved organic matter. In: Kirchman, D. L. (ed.), Microbial Ecology of the Oceans. Wiley-Liss, Inc., New York. p. 121-152.
85. Nishitani, L., Erickson, G. & Chew, K. K. 1985. Role of the parasitic dinoflagellate Amoebophrya ceratii in control of Gonyaulax catenella populations. In: Anderson, D. M., White, A. W. & Baden, D. G. (ed.), Toxic Dinoflagellates. Elsevier Sci. Publ. Co., Inc., New York. p. 225-230.
86. Nishitani, L., Hood, R., Wakeman, J. & Chew, K. K. 1984. Potential importance of an endoparasite of Gonyaulax in paralytic shellfish poisoning outbreaks. In: Ragelis, E. P. (ed.), Seafood Toxins. ACS Symposium Ser., 262:139-149.
87. Norén, F. 2002. Factors regulating planktonic dinoflagellate populations, with special emphasis on the parasitic dinoflagellate Parvilucifera infectans. Dissertation. Department of Marine Ecology, Göteborg University, Sweden. 83 p. ISBN 91-89677-00-5.
88. Norén, F., Moestrup, Ø. & Rehnstam-Holm, A.-S. 1999. Parvilucifera infectans Norén et Moestrup gen. et sp. nov. (Perkinsozoa phylum nov.): a parasitic flagellate capable of killing toxic microalgae. Europ. J. Protistol., 35:233-254.
89. Norén, F., Moestrup, Ø., Rehnstam-Holm, A.-S. & Larsen, J. 2000. Worldwide occurrence and host specificity of Parvilucifera infectans: a parasitic flagellate capable of killing toxic dinoflagellates. In: Hallegraeff, G. M., Blackburn, S. I., Bolch, C. J. & Lewis, R. J. (ed.), Harmful Algal Blooms 2000. Intergovernmental Oceanographic Commission of UNESCO 2001. p. 481-483.
90. Park, M. G., Cooney, S. K., Kim, J. S. & Coats, D. W. 2002a. Effects of parasitism on diel vertical migration, phototaxis/geotaxis, and swimming speed of the bloom-forming dinoflagellate Akashiwo sanguinea. Aquat. Microb. Ecol., 29:11-18.
91. Park, M. G., Cooney, S. K., Yih, W. H. & Coats, D. W. 2002b. Effects of two strains of the parasitic dinoflagellate Amoebophrya on growth, photosynthesis, light absorption, and quantum yield of bloom-forming dinoflagellates. Mar. Ecol. Prog. Ser., 227:281-292.
92. Pelegrí, S. P., Christaki, U., Dolan, J. & Rassoulzadegan, F. 1998. Particulate and dissolved organic carbon production by the heterotrophic nanoflagellate Pteridomonas danica, Patterson and Fenchel 1985, fed Escherichia coli. Microb. Ecol., 37:276-284.
93. Pongratz, E. 1966. De quelques champignons parasites d'organismes planctoniques du Léman. Schweizer Zeitung Hydrologie Rev. Suisse d'Hydrologie, 28:104-132.
94. Pouchet, G., 1885. Nouvelle contribution à l'histoire des Péridiniens marins. J. Anat. Physiol., Paris, 21:28-88.
95. Proctor, L. M. 1997. Advances in the study of marine viruses. Microsc. Res. Tech., 37:136-161.
96. Raghukumar, S. 2002. Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Europ. J. Protistol., 38:127-145.
97. Reynolds, C. S. 1973. The seasonal periodicity of planktonic diatoms in a shallow eutrophic lake. Freshwater Biol., 3:89-110.
98. Reynolds, C. S. 1984. The Ecology of Freshwater Phytoplankton. Cambridge Studies in Ecology. Cambridge Univ. Press, Cambridge.
99. Salomon, P. S., Janson, S. & Granéli, E. 2003. Parasitism of Dinophysis norvegica by Amoebophrya sp. in the Baltic Sea. Aquat. Microb. Ecol., 33:163-172.
100. Sen, B. 1987. Fungal parasitism of planktonic algae in Shearwater. I. Occurrence of Zygorhizidium affluens Canter on Asterionella formosa Hass. in relation to the seasonal periodicity of the alga. Archiv Hydrobiol. (Suppl.), 76:101-127.
101. Sen, B. 1988a. Fungal parasitism of planktonic algae in Shearwater. IV. Parasitic occurrence of a new chytrid species of the blue-green alga Microcystis aerigunosa Kuetz. emend. Elenkin. Archiv Hydrobiol. (Suppl.), 79:177-184.
102. Sen, B. 1988b. Fungal parasitism of planktonic algae in Shearwater. V. Fungal parasites of the green algae. Archiv Hydrobiol. (Suppl.), 79: 185-205.
103. Sengco, M. R., Coats, D. W., Popendorf, K. J., Erdner, D. L., Gribble, K. E. & Anderson, D. M. 2003. Biological and phylogenetic characterization of Amoebophrya sp. ex Alexandrium tamarense. Abstract. Second Symposium on Harmful Marine Algae in the U.S. p. 57.
104. Shibata, A., Kogure, K., Koike, I. & Ohwada, K. 1997. Formation of submicron colloidal particles from marine bacteria by viral infection. Mar. Ecol. Prog. Ser., 155:303-307.
105. Shields, J. D. 1994. The parasitic dinoflagellates of marine crustaceans. Ann. Rev. Fish Dis., 4:241-271.
106. Shin, E.-Y. 1999. A taxonomical study on the thecate dinoflagellates of Korean coastal waters. Dissertation. Department of Oceanography, Seoul National University, Korea. 240 p.
107. Sicko-Goad, L. & Walker, G. 1979. Viroplasm and large virus-like particles in the dinoflagellate Gymnodinium uberrium. Protoplasma, 99:203-210.
108. Silva, E. S. 1978. Endonuclear bacteria in two species of dinoflagellates. Protistologica, 14:113-119.
109. Silva, E. S. 1990. Intracellular bacteria: the origin of dinoflagellate toxicity. JEPTO, 10:124-128.
110. Silva, E. S. & Franca, S. 1985. The association dinoflagellate- bacteria: their ultrastructural relationship in two species of dinoflagellates. Protistologica, 21:429-446.
111. Sommer, U., Wedemeyer, C. & Lowsky, B. 1984. Comparison of potential growth rates of Ceratium hirundinella with observed population density changes. Hydrobiologia, 109:159-164.
112. Soyer, M. O. 1978. Particules de type viral et filaments trichocystoides chez les Dinoflagelles. Protistologica, 14:53-58.
113. Steidinger, K. A. & Vargo, G. A. 1988. Marine dinoflagellate blooms: dynamics and impacts. In: Lembi, C. A. & Wunland, J. R. (ed.), Algae and Human Affairs. Cambridge Univ. Press, Cambridge. p. 373-401.
114. Strom, S. L., Benner, R., Ziegler, S. & Dagg, M. J. 1997. Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol. Oceanogr., 42:1364-1374.
115. Tarutani, K., Nagasaki, K., Itakura, S. & Yamaguchi, M. 2001. Isolation of a virus infecting the novel shellfish-killing dinoflagellate Heterocapsa circularisquama. Aquat. Microb. Ecol., 23:103-111.
116. Taylor, F. J. R. 1968. Parasitism of the toxin-producing dinoflagellate Gonyaulax catenella by the endoparasitic dinoflagellate Amoebophrya ceratii. J. Fish. Res. Bd. Canada, 25:2241-2245.
117. Teegarden, G. J., Campbell, R. G. & Durbin, E. G. 2001. Zooplankton feeding behavior and particle selection in natural plankton assemblages containing toxic Alexandrium spp. Mar. Ecol. Prog. Ser., 218: 213-226.
118. Tester, P. A. & Steidinger, K. A. 1997. Gymnodinium breve red tide blooms: initiation, transport, and consequences of surface circulation. Limnol. Oceanogr., 42:1023-1038.
119. Tillmann, U. & Uwe, J. 2002. Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defense mechanism independent of PSP-toxin content. Mar. Ecol. Prog. Ser., 230:47-58.
120. Toth, G., Norén, F., Selander, E. & Pavia, H. 2001. Parasite-induced morphological defense in a dinoflagellate through water-borne chemical cues. Abstract 189. Phycologia, 40(Suppl.):59.
121. Uppalapati, S. R. & Fujita, Y. 2000. Carbohydrate regulation of attachment, encystment, and appressorium formation by Pythium porphyae (Oomycota) zoospores on Porphyra yezoensis (Rhodophyta). J. Phycol., 36:359-366.
122. van Donk, E. 1989. The role of fungal parasites in phytoplankton succession. In: Sommer, U. (ed.), Plankton Ecology. Springer-Verlag, Berlin. p. 171-194.
123. van Donk, E. & Bruning, K. 1995. Effects of fungal parasites on planktonic algae and the role of environmental factors in the fungus-alga relationship. In: Wiessner, W., Schnepf, E. & Starr, R. (ed.), Algae, Environment and Human Affairs. Biopress Ltd., Bristol. p. 223-234.
124. van Donk, E. & Ringelberg, J. 1983. The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen (The Netherlands). Freshwater Biol., 13:241-251.
125. Wakeman, J. S. & Nishitani, L. 1981. Growth and decline of Gonyaulax catenella bloom associated with parasitism. J. Shellfish Res., 2:122.
126. Weinbauer, M. G. & Peduzzi, P. 1995. Effect of virus-rich high molecular weight concentrates of seawater on the dynamics of dissolved amino acids and carbohydrates. Mar. Ecol. Prog. Ser., 127:245-253.
127. Williams, P. J. leB. 1990. The importance of losses during microbial growth: commentary on the physiology, measurement, and ecology of the release of dissolved organic material. Mar. Microb. Food Webs, 4:175-206.
128. Wilson, W. H., Francis, I., Ryan, K. & Davy, S. K. 2001. Temperature induction of viruses in symbiotic dinoflagellates. Aquat. Microb. Ecol., 25:99-102.
129. Yih, W. & Coats, D. W. 2000. Infection of Gymnodinium sanguineum by the dinoflagellate Amoebophrya sp.: Effect of nutrient environment on parasite generation time, reproduction, and infectivity. J. Eukaryot. Microbiol., 47:504-510.
130. Youngman, R. E., Johnson, D. & Farley, M. R. 1976. Factors influencing phytoplankton growth and succession in Farmoor Reservoir. Freshwater Biol., 6:253-263.