Interactions between planktonic microalgae and protozoan grazers

Journal of Eukaryotic Microbiology

Volumn 51, Issue 2, 2004, Pages 156-168

  Tillmann, Urban ^a  

^a ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

Author keywords

Bloom control; Defense mechanisms; Grazing; Interaction; Microalgae; Protozoa

Indexed keywords

SEA WATER; WATER;

ALGAL BLOOM; BIOLOGICAL CONTROL; GRAZING; PROTOZOAN;

ALGA; ANIMAL; CONFERENCE PAPER; ECOSYSTEM; EUTROPHICATION; FOOD CHAIN; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; PHYTOPLANKTON; POPULATION DYNAMICS; PROTOZOON; ZOOPLANKTON;

ALGAE; ANIMALS; ECOSYSTEM; EUTROPHICATION; FOOD CHAIN; PHYTOPLANKTON; POPULATION DYNAMICS; PROTOZOA; SEAWATER; WATER; WATER MICROBIOLOGY; ZOOPLANKTON;

ALGAE; ANIMALIA; PROTISTA; PROTOZOA;

EID: 1942441383     PISSN: 10665234     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1550-7408.2004.tb00540.x     Document Type: Conference Paper

References (211)

1. Abrahams, M. V. & Townsend, L. D. 1993. Bioluminescense in dinoflagellates: a test of the Burglar alarm hypothesis. Ecology, 74:258-260.
2. Admiraal, W. & Venekamp, L. A. H. 1986. Significance of tintinnid grazing during blooms of Phaeocystis pouchetii (Haptophyceae) in Dutch coastal waters. Neth. J. Sea Res., 20:61-66.
3. Aelion, C. M. & Chisholm, S. W. 1985. Effect of temperature on growth and ingestion rates of Favella sp. J. Plankton Res., 7:821-830.
4. Agatha, S. & Riedel-Lorjé, J. 1998. Morphology, infraciliature, and ecology of some strobilidiine ciliates (Ciliophora, Oligotrichea) from coastal brackish water basins of Germany. Europ. J. Prostistol., 34: 10-17.
5. Andersen, P. & Sörensen, H. M. 1986. Population dynamics and trophic coupling in pelagic microorganisms in eutrophic coastal waters., Mar. Ecol. Prog. Ser., 33:99-109.
6. Anderson, D. M. 1990. Toxin variability in Alexandrium species. In: Granéli, E., Sundström, B., Edler, L. & Anderson, D. M. (ed.), Toxic Marine Phytoplankton. Elsevier, New York. p. 41-51.
7. Anderson, D. M. & Stolzenbach, K. D. 1985. Selective retention of two dinoflagellates in a well-mixed coastal embayment: the importance of diel migration and surface avoidance. Mar. Ecol. Prog. Ser., 25: 39-50.
8. Archer, S. D., Leakey, R. J. G., Burkill, P. H. & Sleigh, M. 1996. Microbial dynamics in coastal waters of East Antarctica: herbivory by heterotrophic dinoflagellates. Mar. Ecol. Prog. Ser., 139:239-255.
9. Ban, S., Burns, C., Castel, J., Chaudron, Y., Christou, E., Escribano, R., Umani, S. F., Gasparini, S., Ruiz, F. G., Hoffmeyer, M., Ianora, A., Kang, H. K., Laabir, M., Lacoste, A., Miralto, A., Ning, X., Poulet, S., Rodriguez, V., Runge, J., Shi, J., Starr, M., Uye, S. & Wang, Y. 1997. The paradox of diatom-copepod interactions. Mar. Ecol. Prog. Ser., 157:287-293.
10. Banse, K. 1992. Grazing, temporal changes of phytoplankton concentrations, and the microbial loop in the open sea. In: Falkowski, P. G. & Woodhead, A. D. (ed.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum Press, New York. p. 409-440.
11. Beers, J. R. & Stewart, G. L. 1971. Micro-zooplankton in the plankton communities of the upper waters of the eastern tropical Pacific. Deep Sea Res., 18:861-883.
12. Bell, G. 1988. Sex and Death in Protozoa. Cambridge University Press, Cambridge, 199 p.
13. Berdalet, E. & Estrada, M. 1993. Effects of turbulence on several dinoflagellate species. In: Smayda, T. J. & Shimizu, Y. (ed.), Toxic Phytoplankton Blooms in the Sea. Elsevier Science Publishers, Amsterdam. p. 737-740.
14. Bernard, C. & Rassoulzadegan, F. 1990. Bacteria or microflagellates as a major food source for marine ciliates: possible implications for the microzooplankton. Mar. Ecol. Prog. Ser., 64:147-155.
15. Biecheler, B. 1952. Recherches sur les Peridiniens. Bull. Biol. Fr. Belg., Suppl., 36:1-149.
16. Bjornsen, P. K. & Nielsen, T. G. 1991. Decimeter scale heterogeneity in the plankton during a pycnocline bloom of Gyrodinium aureolum. Mar. Ecol. Prog. Ser., 73:263-267.
17. Bockstahler, K. R. & Coats, D. W. 1993a. Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Mar. Biol., 116:477-487.
18. Bockstahler, K. R. & Coats, D. W. 1993b. Spatial and temporal aspects of mixotrophy in Chesapeake Bay dinoflagellates. J. Eukaryot. Microbiol., 40:49-60.
19. Bralewska, J. M. & Witek, Z. 1995. Heterotrophic dinoflagellates in the ecosystem of the Gulf of Gdansk. Mar. Ecol. Prog. Ser., 117:241-248.
20. Broglio, E., Johansson, M. & Jonsson, P. R. 2001. Trophic interaction between copepods and ciliates: effects of prey swimming behavior on predation risk. Mar. Ecol. Prog. Ser., 179:179-186.
21. Bursa, A. S. 1961. The annual oceanographic cycle at Igloolik in the Canadian Arctic. II. The phytoplankton. J. Fish. Res. Bd. Can., 18: 563-615.
22. Buskey, E. J. 1997. Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Mar. Ecol. Prog. Ser., 153:77-89.
23. Buskey, E. J. & Stoecker, D. K. 1988. Locomotory patterns of the planktonic ciliate Favella sp.: adaptations for remaining within food patches. Bull. Mar. Sci., 43:783-796.
24. Buskey, E. J. & Stoecker, D. K. 1989. Behavioral responses of the marine tintinnid Favella sp. to phytoplankton: influence of chemical, mechanical and photic stimuli. J. Exp. Mar. Biol. Ecol., 132:1-16.
25. Buskey, E. J., Coulter, C. J. & Brown, S. L. 1994. Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi. Mar. Biol., 121:373-380.
26. Capriulo, G. M., Sherr, E. B. & Sherr, B. F. 1991. Trophic behavior and related community feeding activity of heterotrophic protists. In: Reid, P. C., Turley, C. M. & Burkill, P. H. (ed.), Protozoa and Their Role in Marine Processes. Springer Verlag, New York. p. 219-265.
27. Carlsson, P., Granéli, E. & Olsson, P. 1990. Grazer elimination through poisoning: one of the mechanisms behind Chrysochromulina polylepis blooms? In: Granéli, E., Sundström, B., Edler, L. & Anderson, D. M. (ed.), Toxic Marine Phytoplankton. Elsevier, New York. p. 116-122.
28. Carmichael, W. W. 1994. The toxins of cyanobacteria. Sci. Am., 1:64-72.
29. Caron, D. A., Lim, E. L., Kunze, E. M., Cosper, E. M. & Anderson, D. M. 1989. Trophic interactions between nano-microzooplankton and the "brown tide". In: Cosper, E. M., Bricelj, V. M. & Carpenter, E. J. (ed.), Novel Phytoplankton Blooms: Causes and Impacts of Recurrent Brown Tides and Other Unusual Blooms. Springer Verlag, Berlin. p. 265-294.
30. Carreto, J. I., Benavides, H. R., Negri, R. M. & Glorioso, P. D. 1986. Toxic red-tide in the Argentine Sea. Phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavata in a frontal area. J. Plankton Res., 8:15-28.
31. Cembella, A. D. 1998. Ecophysiology and metabolism of paralytic shellfish toxins in marine microalgae. In: Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algal Blooms. Springer Verlag, Berlin/Heidelberg/New York. p. 381-403.
32. Cembella, A. D., Therriault, J. C. & Béland, P. 1988. Toxicity of cultured isolates and natural populations of Protogonyaulax tamarensis from the St. Lawrence Estuary. J. Shellfish Res., 7:611-621.
33. Chang, F. H., Anderson, D. M., Kulis, D. M. & Till, D. G. 1997. Toxin production of Alexandrium minutum (Dinophyceae) from the Bay of Plenty, New Zealand. Toxicon, 35:393-409.
34. Chen, K. M. & Chang, J. 1999. Influence of light intensity on the ingestion rate of a marine ciliate, Lohmaniella sp. J. Plankton Res., 21:1791-1798.
35. Cho, H. J. & Matsuoka, K. 2000. Cell lysis of a phagotrophic dinoflagellate, Polykrikos kofoidii feeding on Alexandrium tamarense. Plankton Biol. Ecol., 47:134-136.
36. Coats, D. W. 1999. Parasitic life styles of marine dinoflagellates. J. Eukaryot. Microbiol., 46:402-409.
37. 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.
38. Cullen, J. J. & MacIntyre, J. G. 1998. Behavior, physiology and the niche of depth-regulating phytoplankton. In: Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algal Blooms. Springer Verlag, Berlin/Heidelberg/New York. p. 559-579.
39. Dale, T. & Dahl, E. 1987a. Mass occurrence of planktonic oligotrichous ciliates in a bay in southern Norway. J. Plankton Res., 9:871-879.
40. Dale, T. & Dahl, E. 1987b. A red tide in southern Norway caused by mass occurrence of the planktonic ciliate Tiarina fusus. Fauna, 40: 98-103.
41. Dolan, J. R. & Simek, K. 1997. Processing of ingested matter in Strombidium sulcatum, a marine ciliate (Oligotrichida). Limnol. Oceanogr., 42:393-397.
42. Drebes, G. & Schnepf, E. 1998. Gyrodinium undulans Hulburt, a marine dinoflagellate feeding on the bloom-forming diatom Odontella aurita, an on copepod and rotifer eggs. Helgoländer Meeresunters., 52:1-14.
43. Edvardsen, B. 1993. Toxicity of Chrysochromulina species (Prymnesiophyceae) to the brine shrimp, Artemia salina. In: Smayda, T. J. & Shimizu, Y. (ed.), Toxic Phytoplankton Bloom in the Sea. Elsevier Science Publisher, Amsterdam. p. 681-686.
44. Edvardsen, B. & Paasche, E. 1998. Bloom dynamics and physiology of Prymnesium and Chrysochromulina. In: Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algae Blooms. Springer Verlag, Belin/Heidelberg/New York. p. 193-208.
45. Egloff, D. A. 1986. Effects of Olistodiscus luteus on the feeding and reproduction of the marine rotifer Synchaeta cecilia. J. Plankton Res., 8:263-274.
46. Elbrächter, M. 1991. Food uptake mechanisms in phagotrophic dinoflagellates and classification. In: Patterson, D. J. & Larsen, J. (ed.), The Biology of Free-living Heterotrophic Flagellates. Clarendon Press, Oxford. p. 303-312.
47. Elbrächter, M. & Qi, Y. Z. 1998. Aspects of Noctiluca (Dinophyceae) population dynamics. In: Anderson, D. A., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algae Blooms. Springer, Berlin/Heidelberg/New York. p. 315-335.
48. Fauré-Fremiet, E. 1948. Le rythme de marée du Strombidium oculatum Gruber. Bulletin biologique de la France et de la Belgique, 82:3-23.
49. Fukami, K., Watanabe, A., Fujita, S., Yamaoka, K. & Nishijima, T. 1999. Predation on naked protozoan microzooplankton by fish larvae. Mar. Ecol. Prog. Ser., 185:285-291.
50. Gentien, P. 1998. Bloom dynamics and ecophysiology of the Gymnodinium mikimotoi species complex. In: Anderson, D. A., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algae Blooms. Springer, Berlin/Heidelberg/New York. p. 155-173.
51. Gifford, D. J. 1985. Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotricha). Mar. Ecol. Prog. Ser., 23:257-267.
52. Goldman, J. C., Dennett, M. R. & Gordin, H. 1989. Dynamics of herbivorous grazing by the heterotrophic dinoflagellate Oxyrrhis marina. J. Plankton Res., 11:391-407.
53. Gomez, F. & Gorsky, G. 2003. Annual microplankton cycles in Villefranche Bay, Ligurian Sea, NW Mediterranean. J. Plankton Res., 25: 323-339.
54. Hansen, F. C. 1995a. Trophic interaction between zooplankton and Phaeocystis cf. globosa. Helgoländer Meeresunters., 49:283-293.
55. Hansen, F. C. & van Boekel, W. H. M. 1991. Grazing pressure of the calanoid copepod Temora longicornis on a Phaeocystis-dominated spring bloom in a Dutch tidal inlet. Mar. Ecol. Prog. Ser., 78:123-129.
56. Hansen, F. C., Witte, H. J. & Passarge, J. 1996. Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and the preference for calcified Emiliania huxlyi cells. Aquat. Microb. Ecol., 10: 307-313.
57. Hansen, F. C., Reckermann, M., Klein Breteler, W. C. M. & Riegman, R. 1993. Phaeocystis blooming enhanced by copepod predation on protozoa: evidence from incubation experiments. Mar. Ecol. Prog. Ser., 102:51-57.
58. Hansen, P. J. 1989. The red tide dinoflagellate Alexandrium tamarense: effects on behavior and growth of a tintinnid ciliate. Mar. Ecol. Prog. Ser., 53:105-116.
59. Hansen, P. J. 1991a. Dinophysis - a planktonic dinoflagellate genus which can act both as prey and a predator of a ciliate. Mar. Ecol. Prog. Ser., 69:201-204.
60. Hansen, P. J. 1991b. Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagic food web. Mar. Ecol. Prog. Ser., 73:253-261.
61. Hansen, P. J. 1992. Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar. Biol., 114:327-334.
62. Hansen, P. J. 1995b. Growth and grazing response of a ciliate feeding on the red tide dinoflagellate Gyrodinium aureolum in monocultures and in mixture with a non-toxic alga. Mar. Ecol. Prog. Ser., 121:65-72.
63. Hansen, P. J. 1998. Phagotrophic mechanisms in prey selection in mixotrophic phytoflagellates. In: Anderson, D. M., Cembella, A. D. & Hallegraeff, G. M. (ed.), Physiological Ecology of Harmful Algal Blooms. Springer Verlag, Berlin/Heidelberg/New York. p. 525-537.
64. Hansen, P. J. & Calado, A. J. 1999. Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J. Eukaryot. Microblol., 46: 382-389.
65. 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. Phycol., 28: 597-603.
66. Harumoto, T. 1994. The role of trichocyst discharge and backward swimming in escape behavior of Paramecium from Dileptus margaritifer. J. Eukaryot. Microblol., 41:560-564.
67. Heinbokel, J. F. 1978. Studies on the functional role of tintinnids in the southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar. Biol., 47:177-189.
68. Holmes, R. W., Williams, P. M. & Eppley, R. W. 1967. Red water in La Jolla Bay, 1964-1966. Limnol. Oceanogr., 12:503-512.
69. Holm-Hansen, O., Taylor, F. J. R. & Barsdate, R. J. 1970. A ciliate red tide at Barrow, Alaska. Mar. Biol., 7:37-46.
70. Jacobson, D. M. & Anderson, D. M. 1986. Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J. Phycol., 22:249-258.
71. Jacobson, D. M. & Anderson, D. M. 1993. Growth and grazing rates of Protoperidinium hirobis Abe, a thecate heterotrophic dinoflagellate. J. Plankton Res., 15:723-736.
72. Jacobson, D. M. & Anderson, D. M. 1996. Widespread phagocytosis of ciliates and other protists by mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol., 32:279-285.
73. Jakobsen, H. H. 2001. Escape response of planktonic protists to fluid mechanical signals. Mar. Ecol. Prog. Ser., 214:67-78.
74. Jakobsen, H. H. 2002. Escape of protists in predator-generated feeding currents. Aquat. Microb. Ecol., 26:271-281.
75. Jakobsen, H. H. & Hansen, P. J. 1997. Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum - a comparative study. Mar. Ecol. Prog. Ser., 158:75-86.
76. Jeong, H. J. 1999. The ecological role of heterotrophic dinoflagellates in marine plankton community. J. Eukaryot. Microblol., 46:390-396.
77. Jeong, H. J. 2001. Developing a method of controlling the outbreak and maintenance of red tides using mass-cultured grazers. Abstract. Aquatic Science Meeting. American Society of Limnology and Oceanography. Albuquerque, New Mexico, USA. p. 74.
78. Jeong, H. J. & Latz, M. I. 1994. Growth and grazing rates of the heterotrophic dinoflagellate Protoperidinium spp. on red tide dinoflagellates. Mar. Ecol. Prog. Ser., 106:173-185.
79. Jeong, H. J. & Shim, J. H. 1996. Interactions between the red-tide dinoflagellate Gymnodinium sanguineum and its microzooplankton grazers. In: Yasumoto, T., Oshima, Y. & Fukuyo, Y. (ed.), Harmful and Toxic Algal Blooms. Intergovernmental Oceanographic Commission of UNESCO. p. 377-380.
80. Jeong, H. J., Shim, J. H., Lee, C. W., Kim, J. S. & Koh, S. M. 1999a. Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol., 46:69-76.
81. Jeong, H. J., Yoon, J. Y., Kim, J. S., Yoo, Y. D. & Seong, K. A. 2002a. Growth and grazing rates of the prostomatic ciliate Tiarina fusus on red-tide and toxic algae. Aquat. Microb. Ecol., 28:289-297.
82. Jeong, H. J., Kim, S. K., Kim, J. S., Kim, S. T., Yoo, Y. D. & Yoon, J. H. 2001a. Growth and grazing rates of the heterotrophic dinoflagellate Polykrikos kofoidii on red-tide and toxic dinoflagellates. J. Eukaryot. Microbiol., 48:298-308.
83. Jeong, H. J., Shim, J. H., Kim, J. S., Park, J. Y., Lee, C. W. & Lee, Y. 1999b. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser., 176:263-277.
84. Jeong, H. J., Kang, H., Shim, J. H., Park, J. K., Kim, J. S., Song, J. Y. & Choi, H. J. 2001b. Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepod Acartia spp. Mar. Ecol. Prog. Ser., 218: 77-86.
85. Jeong, H. J., Park, K. H., Kim, J. S., Kang, H., Kim, C. H., Choi, H. J., Kim, Y. S., Park, J. Y. & Park, M. G. 2003a. Reduction in the toxicity of the dinoflagellate Gymnodinium catenatum when fed on by the heterotrophic dinoflagellate Polykrikos kofoidii. Aquat. Microb. Ecol., 31:307-312.
86. Jeong, H. J., Kim, J. S., Yoo, Y. D., Kim, S. T., Kim, T. H., Park, M. G., Lee, C. H., Seong, K. A., Kang, N. S. & Shim, J. H. 2003b. Feeding by the heterotrophic dinoflagellate Oxyrrhis marina on the red-tide raphidophyte Heterosigma akashiwo: a potential biological method to control red tides using mass-cultured grazers. J. Eukaryot. Microbiol., 50:274-282.
87. Jeong, H. J., Kim, H. R., Kim, K. I., Kim, K. Y., Park, K. H., Kim, S. T., Yoo, Y. D., Song, J. Y., Kim, J. S., Seong, K. A., Yih, W. H., Pae, S. J., Lee, C. H., Huh, M. D. & Lee, S. H. 2002b. NaOCl produced by electrolysis of natural seawater as a potential method to control marine red tide dinoflagellates. Phycologia, 41:643-656.
88. Johansson, N. 2000. Ecological implications of the production of toxic substances by fish-killing phytoplankton species grown under variable N:P-ratios. Dissertation. Lund University, Sweden, 106 p.
89. Johansson, N. & Granéli, E. 1999. Cell density, chemical composition and toxicity of Chrysochromulina polylepis (Haptophyta) in relation to different N:P supply ratios. Mar. Biol., 135:209-217.
90. John, U., Tillmann, U. & Medlin, L. 2002. A comparative approach to study inhibition of grazing and lipid composition of a toxic and non-toxic clone of Chrysochromulina polylepis (Prymnesiophyceae). Harmful Algae, 1:45-57.
91. Johnson, M. D., Rome, M. & Stoecker, D. K. 2003. Microzooplankton grazing on Prorocentrum minimum and Karlodinium micrum in Chesapeake Bay. Limnol. Oceanogr., 48:238-248.
92. Jones, H. L. J., Leadbeater, B. S. C., & Green, J. C. 1993. Mixotrophy in marine species of Chrysochromulina (Prymnesiophyceae): ingestion and digestion of a small green flagellate. J. Mar. Biol. Assoc. U.K., 73:283-296.
93. Jonsson, P. R. 1986. Particle-size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar. Ecol. Prog. Ser., 33:265-277.
94. Kamiyama, T. 1997. Growth and grazing response of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsa circularisquama. Mar. Biol., 128:509-515.
95. Kamiyama, T. & Arima, S. 1997. Lethal effect of the dinoflagellate Heterocapsa circularisquama upon the tintinnid ciliate Favella taraikaensis. Mar. Ecol. Prog. Ser., 160:27-33.
96. Kamiyama, T. & Arima, S. 2001. Feeding characteristics of two tintinnid ciliate species on phytoplankton including harmful species: effects of prey size on ingestion rates and selectivity. J. Exp. Mar. Biol. Ecol., 257:281-296.
97. Kiorboe, T. & Titelman, J, 1998. Feeding, prey selection and prey encounter mechanisms in the heterotrophic dinoflagellate Noctiluca scintillans. J. Plankton Res., 20:1615-1636.
98. Klein Breteler, W. C. M. 1980. Continuous breeding of marine pelagic copepods in the presence of heterotrophic dinoflagellates. Mar. Ecol. Prog. Ser., 2:229-233.
99. Klein Breteler, W. C. M., Schogt, N., Baas, M., Schouten, S. & Kraay, G. W. 1999. Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar. Biol., 135: 191-198.
100. Klekowski, R. Z. & Tumantseva, N. I. 1981. Respiratory metabolism of three marine infusoria: Strombidium sp., Tiarina fusus and Diophrys sp. Ecologica Polska, 29:271-282.
101. Landry, M. R. & Hassett, R. P. 1982. Estimating the grazing impact of marine micro-zooplankton. Mar. Biol., 67:283-288.
102. Laybourn-Parry, J. 1992. Protozoan Plankton Ecology. Chapman & Hall, London, New York. 231 p.
103. Legrand, C., Regefors, K., Fistarol, G. O. & Granéli, E. 2003. Allelopathy in phytoplankton - biochemical, ecological and evolutionary aspects. Phycologia, 42:406-419.
104. Lessard, E. J. 1991. The trophic role of heterotrophic dinoflagellates in diverse marine environments. Mar. Microb. Food Webs, 5:49-58.
105. Levandowski, M. & Hauser, D. C. R. 1978. Chemosensory responses of swimming algae and protozoa. Int. Rev. Cytol., 53:145-210.
106. Levinsen, H. & Nielsen, T. G. 2002. The trophic role of marine pelagic ciliates and heterotrophic dinoflagellates in arctic and temperate coastal ecosystems: a cross-latitude comparison. Limnol. Oceanogr., 47:427-439.
107. Li, A., Stoecker, D. K., Coats, D. W. & Adam, E. J. 1996. Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates. Aquat. Microb. Ecol., 10:139-147.
108. Maneiro, I., Frangópulos, M., Guisande, C., Fernández, M., Reguera, B. & Rivero, I. 2000. Zooplankton as a potential vector of diarrhetic shellfish poisoning toxics through the food web. Mar. Ecol. Prog. Ser., 201:155-163.
109. Matsuoka, K., Cho, H. J. & Jacobson, D. M. 2000. Observation of the feeding behavior and growth rates of the heterotrophic dinoflagellate Polykrikos kofoidii (Polykrikaceae, Dinophyceae). Phycologia, 39: 82-86.
110. Matsuyama, Y., Miyamoto, M. & Kotani, Y. 1999. Grazing impact of the heterotrophic dinoflagellate Polykrikos kofoidii on a bloom of Gymnodinium catenatum. Aquat. Microb. Ecol., 17:91-98.
111. Merrel, J. R. & Stoecker, D. K. 1998. Differential grazing on protozoan microplankton by developmental stages of the calanoid copepod Eurytemora affinis Poppe. J. Plankton Res., 20:289-304.
112. Miralto, A., Barone, G., Romano, G., Poulet, S. A., Ianora, A., Russo, G. L., Buttino, I., Mazzarella, G., Laabir, M., Cabrini, M. & Giacobbe, M. G. 1999. The insidious effect of diatoms on copepod reproduction. Nature, 402:173-176.
113. Miyake, A. & Harumoto, T. 1996. Defensive function of trichocysts in Paramecium against the predatory ciliate Monodinium balbiani. Europ. J. Protistol., 32:128-133.
114. Montagnes, D. J. S. 1996. Growth response of planktonic ciliates in the genera Strobilidium and Strombidium. Mar. Ecol. Prog. Ser., 130: 241-254.
115. Montagnes, D. J. S. & Humphrey, E. 1998. A description of occurrence and morphology of a new species of red-water-forming Strombidium (Spirotrichea, Oligotricha). J. Eukaryot. Microbiol., 45:502-506.
116. Montagnes, D. J. S. & Lessard, E. J. 1999. Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms. Aquat. Microb. Ecol., 20:167-181.
117. Montagnes, D. J. S., Berger, J. D. & Taylor, F. J. R. 1996. Growth rate of the marine planktonic ciliate Strombidinopsis cheshiri Snyder and Ohman as a function of food concentration and interclonal variability. J. Exp. Mar. Biol. Ecol., 206:121-132.
118. Nakamura, Y. 1998. Growth and grazing of a large heterotrophic dinoflagellate, Noctiluca scintillans, in laboratory cultures. J. Plankton Res., 20:1711-1720.
119. Nakamura, Y., Suzuki, S. & Hiromi, J. 1995a. Growth and grazing of a naked heterotrophic dinoflagellate, Gyrodinium dominans. Aquat. Microb. Ecol., 9:157-164.
120. Nakamura, Y., Suzuki, S. Y. & Hiromi, J. 1995b. Population dynamics of heterotrophic dinoflagellates during a Gymnodinium mikimotoi red tide in the Seto Inland Sea. Mar. Ecol. Prog. Ser., 125:269-277.
121. Nakamura, Y., Suzuki, S. & Hiromi, J. 1996. Development and collapse of a Gymnodinium mikimotoi red tide in the Seto Inland Sea. Aquat. Microb. Ecol., 10:131-137.
122. Nakamura, Y., Yamazaki, Y. & Hiromi, J. 1992. Growth and grazing of a heterotrophic dinoflagellate, Gyrodinium dominans, feeding on a red-tide flagellate, Chattonella antiqua. Mar. Ecol. Prog. Ser., 82: 275-279.
123. Naustvoll, L. J. 1998. Growth and grazing by the thecate heterotrophic dinoflagellate Diplopsalis lenticula (Diplopsalidaceae, Dinophyceae). Phycologia, 37:1-9.
124. Naustvoll, L. J. 2000a. Prey-size spectra and food preferences in thecate heterotrophic dinoflagellates. Phycologia, 39:187-198.
125. Naustvoll, L. J. 2000b. Prey size spectra in naked heterotrophic dinoflagellates. Phycologia, 39:448-455.
126. Needler, A. B. 1949. Paralytic shellfish poisoning and Gonyaulax tamarensis. J. Fish. Res. Bd. Can., 7:490-504.
127. Nielsen, T. G., Kiorboe, T. & Bjornsen, P. K. 1990. Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar. Ecol. Prog. Ser., 62:21-35.
128. Nygaard, K. & Tobiesen, A. 1993. Bacterivory in algae: a survival strategy during nutrient limitation. Limnol. Oceanogr., 38:273-279.
129. Paasche, E. & Kristiansen, S. 1982. Ammonium regeneration by microzooplankton in the Oslofjord. Mar. Biol., 69:55-63.
130. Paranjape, M. A. 1980. Occurrence and significance of resting cysts in a hyaline tintinnid, Helicostomella subulata (Ehre.) Jorgensen. J. Exp. Mar. Biol. Ecol., 48:23-33.
131. Parkhill, J. P. & Cembella, A. D. 1999. Effects of salinity, light and inorganic nitrogen on growth and toxigenity of the marine dinoflagellate Alexandrium tamarense from northeastern Canada. J. Plankton Res., 21:939-955.
132. Pedersen, M. F. & Hansen, P. J. 2003. Effects of high pH on the growth and survival of six marine heterotrophic protists. Mar. Ecol. Prog. Ser., 33:33-41.
133. Pohnert, G. 2002. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol., 129:103-111.
134. Pohnert, G., Lumineau, O., Cueff, A., Adolph, S., Codevant, C., Lange, M. & Poulet, S. 2002. Are volatile unsaturated aldehydes from diatoms the main line of chemical defense against copepods? Mar. Ecol. Prog. Ser., 245:33-45.
135. Prakash, A. 1963. Source of paralytic shellfish toxin in the Bay of Fundy. J. Fish. Res. Bd. Can., 20:983-996.
136. Rassoulzadegan, F. 1977. Evolution annuelle des ciliés pélagiques en Méditeranée nord-occidentale. Ciliés oligotriches "non-tintinnides" (Oligotrichina). Ann. Inst. Océanogr., Paris, 53:125-134.
137. Rassoulzadegan, F. 1982. Dependence of grazing rate, gross growth efficiency and food size range on temperature in a pelagic oligotrichous ciliate Lohmaniella spiralis Leeg., fed on naturally occurring particulate matter. Ann. Inst. Océanogr., Paris, 58:177-184.
138. Repak, A. J. 1983. Suitability of selected marine algae for growing the marine heterotrich ciliate Fabrea salina. J. Protozool., 30:52-54.
139. Richardson, K. 1997. Harmful or exceptional phytoplankton blooms in the marine ecosystem. Adv. Mar. Biol., 31:301-385.
140. Riedel-Lorjé, J. C., Nehring, S., Hesse, K. J. & Agatha, S. 1997. Plankton und Nährstoffe in Brackwasserbecken am Rande des Schleswig-Holsteinischen Wattenmeeres unter besonderer Berúcksichtigung der Ciliaten und Dinoflagellaten-Dauerstadien sowie blútenbildender und toxischer Formen. Federal Environmental Agency, Berlin. 102 p.
141. Rublee, P. A. & Gallegos, C. L. 1989. Use of fluorescently labelled algae (FLA) to estimate microzooplankton grazing. Mar. Ecol. Prog. Ser., 51:221-227.
142. Sampayo, M. A. 1998. Polykrikos kofoidii Chatton predation on Gymnodinium catenatum Graham and its effects. In: Reguera, B., Blanco, J., Fernandez, M. L. & Wyatt, T. (ed.), Harmful Algae. Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO. p. 182-183.
143. Sato, Y., Oda, T., Muramatsu, T., Matsuyama, Y. & Honjo, T. 2002. Photosensitizing hemolytic toxin in Heterocapsa circularisquama, a newly identified harmful red-tide dinoflagellate. Aquat. Toxicol., 56: 191-196.
144. Schmidt, L. E. & Hansen, P. J. 2001. Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Mar. Ecol. Prog. Ser., 216:67-81.
145. Schnepf, E. & Elbrächter, M. 1992. Nutritional strategies in dinoflagellates. A review with emphasis on cell biological aspects. Europ. J. Protistol., 28:3-24.
146. Sengco, M. R., Tugend, K., Kulis, D. M. & Anderson, D. M. 2001. Removal of red-and brown-tide cells using clay flocculation. I. Laboratory culture experiments with Gymnodinium breve and Aureococcus anophagefferens. Mar. Ecol. Prog. Ser., 210:41-53.
147. Sherr, E. B. & Sherr, B. F. 1992. Trophic role of pelagic protists: phagotrophic flagellates as herbivores. Arch. Hydrobiol. Beih. Ergebn. Limnol., 37:165-172.
148. Sherr, E. B. & Sherr, B. F. 1994. Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb. Ecol., 28:223-235.
149. Sieburth, J. M., Smetacek, V. & Lenz, J. 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnol. Oceanogr., 23:1256-1263.
150. Skovgaard, A. 1996a. Engulfment of Ceratium spp. (Dinophyceae) by the thecate photosynthetic dinoflagellate Fragilidium subglobosum. Phycologia, 35:490-499.
151. Skovgaard, A. 1996b. Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing response as functions of light intensity. Mar. Ecol. Prog. Ser., 143:247-253.
152. Skovgaard, A. & Hansen, P. J. 2003. Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins. Limnol. Oceanogr., 48:1161-1166.
153. Skovgaard, A., Hansen, P. J. & Stoecker, D. K. 2000. Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. 1. Effects of phagotrophy and irradiance on photosynthesis and carbon content. Mar. Ecol. Prog. Ser., 201:129-136.
154. Smalley, G. W. & Coats, D. W. 2002. Ecology of the red-tide dinoflagellate Ceratium furca: distribution, mixotrophy, and grazing impact on ciliate populations of Chesapeake Bay. J. Eukaryot. Microbiol., 49:63-73.
155. Smalley, G. W., Coats, D. W. & Adams, E. J. 1999. A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquat. Microb. Ecol., 17:167-179.
156. Smayda, T. J. 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr., 42:1137-153.
157. Smetacek, V. 1981. The annual cycle of protozooplankton in the Kiel Bight. Mar. Biol., 63:1-11.
158. Smetacek, V. 2001. A watery arms race. Nature, 411:745.
159. Spero, H. J. & Morée, M. D. 1981. Phagotrophic feeding and its importance to the life cycle of the holozoic dinoflagellate Gymnodinium fungiforme. J. Phycol., 17:43-51.
160. Stoecker, D. K. 1988. Are marine planktonic ciliates suspension-feeders? J. Protozool., 35:252-255.
161. Stoecker, D. K. & Evans, G. T. 1985. Effects of protozoan herbivory and carnivory in a microplankton food web. Mar. Ecol. Prog. Ser., 25:159-167.
162. Stoecker, D. K. & Guillard, R. R. L. 1982. Effects of temperature and light on the feeding rate of Favella sp. (ciliated protozoa, suborder Tintinnia). Ann. Inst. Oceanogr., Paris, 58:309-318.
163. Stoecker, D. K. & McDowell Capuzzo, J. 1990. Predation on Protozoa: its importence to zooplankton. J. Plankton Res., 12:891-908.
164. Stoecker, D. K. & Michaels, A. E. 1991. Respiration, photosynthesis and carbon metabolism in planktonic ciliates. Mar. Biol., 108:441-447.
165. Stoecker, D., Guillard, R. R. L. & Kavee, R. M. 1981. Selective predation by Favella ehrenbergii (Tintinnida) on and among dinoflagellates. Biol. Bull., 160:136-145.
166. Stoecker, D. K., Stevens, K. & Gustafson, D. E. 2000. Grazing on Pfisteria piscicida by microzooplankton. Aquat. Microb. Ecol., 22: 261-270.
167. Stoecker, D. K., Verity, P. G., Michaels, A. E. & Davis, L. H. 1987. Feeding by larval and post-larval ctenophores on microzooplankton. J. Plankton Res., 9:667-683.
168. Strom, S. L. 1991. Growth and grazing rates of the herbivorous dinoflagellate Gymnodinium sp. from the open subarctic Pacific Ocean. Mar. Ecol. Prog. Ser., 78:103-113.
169. Strom, S. 2002. Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea. Hydrobiologia, 480:41-54.
170. Strom, S. L. & Buskey, E. J. 1993. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr., 38:965-977.
171. Strom, S. L. & Morello, T. A. 1998. Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J. Plankton Res., 20:571-584.
172. 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.
173. Strom, S. L., Brainard, M. A., Holmes, J. L. & Olson, M. B. 2001. Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Mar. Biol., 138:355-368.
174. Strom, S., Wolfe, G. V., Slajer, A., Lambert, A. & Clough, J. 2003a. Chemical defense in the microplankton II: Inhibition of protist feeding by β-dimethylsulfoniopropionate (DMSP). Limnol. Oceanogr., 48:230-237.
175. Strom, S., Wolfe, G. V., Holmes, J., Stecher, H., Shimeneck, C., Lambert, A. & Moreno, E. 2003b. Chemical defense in the microplankton I: Feeding and growth rates of heterotrophic protists on the DMS-producing phytoplankter Emiliania huxleyi. Limnol. Oceanogr., 48: 217-229.
176. Sulkin, S., Lehto, J., Strom, S. & Hutchinson, D. 1998. Nutritional role of protists in the diet of a first stage larvae of the Dungeness crab Cancer magister. Mar. Ecol. Prog. Ser., 169:237-243.
177. Tang, K. W., Jakobsen, H. H. & Visser, A. W. 2001. Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: feeding, growth, and trophic interactions among grazers. Limnol. Oceanogr., 46:1860-1870.
178. Tangen, K. 1980. Brown waters in the Oslofjord, Norway, in September 1979, caused by the toxic Prorocentrum minimum and other dinoflagellates (in Norwegian). Blyttia, 38:145-158.
179. Taniguchi, A. & Kawakami, R. 1985. Feeding activity of a tintinnid ciliate Favella taraikaensis and its variability observed in laboratory cultures. Mar. Microb. Food Webs, 1:17-34.
180. Tanigushi, A. & Takeda, Y. 1988. Feeding rate and behavior of the tintinnid ciliate Favella taraikaensis, observed with a high speed VTR system. Mar. Microb. Food Webs, 3:21-34.
181. Tarran, G. 1991. Aspects of the grazing behavior of the marine dinoflagellate Oxyrrhis marina, Dujardin. Dissertation. University of Southampton, Southampton, England. 188 p.
182. Tarutani, K., Nagasaki, K. & Yamaguchi, M. 2000. Viral impact on total abundance and clonal composition of the harmful bloom-forming phytoplankton Heterosigma akashiwo. Appl. Environ. Microbiol., 66:4916-4920.
183. Teegarden, G. J. & Cembella, A. D. 1996. Grazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: implications for the fate of paralytic shellfish toxins in marine food webs. J. Exp. Mar. Biol. Ecol., 196:145-176.
184. Tester, P. A., Turner, J. T. & Shea, D. 2000. Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish. J. Plankton Res., 22:47-61.
185. Tillmann, U. 1998. Phagotrophy of a plastidic haptophyte, Prymnesium patelliferum. Aquat. Microb. Ecol., 14:155-160.
186. Tillmann, U. 2003. Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum. Aquat. Microb. Ecol., 32:73-84.
187. Tillmann, U. & Hesse, K.-J. 1998. On the quantitative importance of heterotrophic microplankton in the northern German Wadden Sea. Estuaries, 21:585-596.
188. Tillmann, U. & John, U. 2002. Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defense mechanism independent of PSP toxins. Mar. Ecol. Prog. Ser., 230:47-58.
189. Tillmann, U. & Reckermann, M. 2002. Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica. Aquat. Microb. Ecol., 26:247-257.
190. Tobiesen, A. 1991. Growth rates of Heterophrys marina (Heliozoa) on Chrysochromulina polylepis (Prymnesiophyceae). Ophelia, 33:205-212.
191. Turriff, N., Runge, J. A. & Cembella, A. D. 1995. Toxin accumulation and feeding behavior of the planktonic copepod Calanus finmarchicus exposed to the red-tide dinoflagellate Alexandrium excavatum. Mar. Biol., 123:55-64.
192. Uchida, T., Kamiyama, T. & Matsuyama, Y. 1997. Predation by a photosynthetic dinoflagellate Gyrodinium instriatum on loricated ciliates. J. Plankton Res., 19:603-608.
193. Uchida, T., Yamaguchi, M., Matsuyama, Y. & Honjo, T. 1995. The red-tide dinoflagellate Heterocapsa sp. kills Gyrodinium instriatum by cell contact. Mar. Ecol. Prog. Ser., 118:301-303.
194. Ukeles, R. & Sweeney, B. M. 1969. Influence of dinoflagellates trichocysts and other factors on the feeding of Crassostrea virginica larvae on Monochrysis lutheri. Limnol. Oceanogr., 14:403-410.
195. Vardi, A., Schatz, D., Beeri, K., Motro, U., Sukenik, A., Levine, A. & Kaplan, A. 2002. Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake. Curr. Biol., 12:1767-1772.
196. Verity, P. G. 1985. Grazing, respiration, excretion, and growth rates of tintinnids. Limnol. Oceanogr., 30:1268-1282.
197. Verity, P. G. 1988. Chemosensory behavior in marine planktonic ciliates. Bull. Mar. Sci., 43:772-782.
198. Verity, P. G. 1991a. Feeding in planktonic protozoans: evidence for non-random acquisition of prey. J. Protozool., 38:69-76.
199. Verity, P. G. 1991b. Measurement and simulation of prey uptake by marine planktonic ciliates fed plastidic and aplastidic nanoplankton. Limnol. Oceanogr., 36:729-750.
200. Verity, P. G. & Smetacek, V. 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar. Ecol. Prog. Ser., 130:277-293.
201. Verity, P. G. & Stoecker, D. 1982. Effects of Olistodiscus luteus on the growth and abundance of tintinnids. Mar. Biol., 72:79-87.
202. Verity, P. G. & Villareal, T. A. 1986. The relative food value of diatoms, dinoflagellates, flagellates and cyanobacteria for tintinnid ciliates. Arch. Protistenkd., 131:71-84.
203. Watras, C. J., Carcon, V. C., Olson, R. J., Chisholm, S. W. & Anderson, D. M. 1985. The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis. J. Plankton Res., 7:891-908.
204. Weisse, T. & Scheffel-Möeser, U. 1990. Growth and grazing loss rates in single-celled Phaeocystis sp. (Prymnesiophyceae). Mar. Biol., 106: 153-158.
205. White, A. W. 1981. Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish kills. Limnol. Oceanogr., 26:103-109.
206. White, A. W. 1986. High toxin content in the dinoflagellate Gonyaulax excavata in nature. Toxicon, 24:605-610.
207. Wolfe, G. V. 2000. The chemical defense ecology of marine unicellular plankton: constrains, mechanisms, and impacts. Biol. Bull., 198:225-244.
208. Wolfe, G. V. & Steinke, M. 1996. Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnol. Oceanogr., 41:1151-1160.
209. Wolfe, G. V., Steinke, M. & Kirst, G. O. 1997. Grazing-activated chemical defense in a unicellular marine alga. Nature, 387:894-897.
210. Wyatt, T. & Jenkinson, I. R. 1997. Notes on Alexandrium population dynamics. J. Plankton Res., 19:551-575.
211. Yoshinaga, I., Kim, M. C., Katanozaka, N., Imai, I., Uchida, T. & Ishida, Y. 1998. Population structure of algicidal marine bacteria targeting the red tide forming alga Heterosigma akashiwo (Raphidophyceae), determined by restriction fragment length polymorphism analysis of the bacterial 16S ribosomal RNA genes. Mar. Ecol. Prog. Ser., 170:33-44.