Advertisement

Antonie van Leeuwenhoek

, Volume 81, Issue 1–4, pp 293–308 | Cite as

Significance of predation by protists in aquatic microbial food webs

  • Evelyn B. Sherr
  • Barry F. Sherr
Article

Abstract

Predation in aquatic microbial food webs is dominated by phagotrophic protists, yet these microorganisms are still understudied compared to bacteria and phytoplankton. In pelagic ecosystems, predaceous protists are ubiquitous, range in size from 2 μm flagellates to >100 μm ciliates and dinoflagellates, and exhibit a wide array of feeding strategies. Their trophic states run the gamut from strictly phagotrophic, to mixotrophic: partly autotrophic and partly phagotrophic, to primarily autotrophic but capable of phagotrophy. Protists are a major source of mortality for both heterotrophic and autotrophic bacteria. They compete with herbivorous meso- and macro-zooplankton for all size classes of phytoplankton. Protist grazing may affect the rate of organic sinking flux from the euphotic zone. Protist excretions are an important source of remineralized nutrients, and of colloidal and dissolved trace metals such as iron, in aquatic systems. Work on predation by protists is being facilitated by methodological advances, e.g., molecular genetic analysis of protistan diversity and application of flow cytometry to study population growth and feeding rates. Examples of new research areas are studies of impact of protistan predation on the community structure of prey assemblages and of chemical communication between predator and prey in microbial food webs.

bacterivory herbivory microbial food webs pelagic ecosystems phagotrophy protists 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Archer SD, Leakey RJG, Burkill PH, Sleigh MA & Appleby CJ (1996a) Microbial ecology of sea ice at a coastal Antarctic site: community composition, biomass and temporal change. Mar. Ecol. Prog. Ser. 135: 179–195.CrossRefGoogle Scholar
  2. Archer SD, Leakey RJG, Burkill PH & Sleigh MA (1996b) Microbial dynamics in coastal waters of east Antarctica: herbivory by heterotrophic dinoflagellates. Mar. Ecol. Prog. Ser. 139: 239–255.CrossRefGoogle Scholar
  3. Archer, SD, Verity PG & Stefels J (2000) Impact of microzooplankton on the progression and fate of the spring bloom in fjords of northern Norway. Aquat. Microb. Ecol. 22: 27–41.CrossRefGoogle Scholar
  4. Arenovski AL, Lim EL & Caron DA (1995) Mixotrophic nanoplankton in oligotrophic surface waters of the Sargasso Sea may employ phagotrophy to obtain major nutrients. J. Plankton Res. 17: 801–820.CrossRefGoogle Scholar
  5. Azam F, Fenchel T, Field JG, Meyer-Reil RA & Thingstad F (1983) The ecological role of water column microbes in the sea. Mar. Ecol. Prog. Ser. 10: 257–263.CrossRefGoogle Scholar
  6. Barbeau K, Moffett JW, Caron DA, Croot PL & Erdner DL (1996) Role of protozoan grazing in relieving iron limitation of phytoplankton. Nature 380: 61–64.CrossRefGoogle Scholar
  7. Barbeau K, Kujawinski EB & Moffett JW (2001) Remineralization and recycling of iron, thorium and organic carbon by heterotrophic marine protists in culture. Aquat. Microb. Ecol. 24: 69–81.CrossRefGoogle Scholar
  8. Beja O, Aravind L, Koonin EV, Suzuki MT, Hadd A, Nguyen LP, Jovanovich S, Gates CM, Feldman RA, Spudlich JL, Spudlich EN & DeLong EF (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289: 1902–1906.CrossRefPubMedGoogle Scholar
  9. Beja O, Spudlich EN, Spudlich JL, Leclerc M & DeLong EF (2001) Proteorhodopsin phototrophy in the ocean. Nature 411: 786–789.CrossRefPubMedGoogle Scholar
  10. Bernard C, Simpson AGB & Patterson DJ (2000) Some free-living flagellates (Protista) from anoxic habitats. Ophelia 52: 113–114.Google Scholar
  11. Baretta-Bekker JG, Baretta JW & Rasmussen EK (1995) The microbial food web in the European Regional Seas Ecosystem Model. Neth. J. Sea Res. 33: 363–395.CrossRefGoogle Scholar
  12. Blanchot J, Andre J-M, Navarette C, Neveus J & Radenac MH (2001) Picophytoplankton in the equatorial Pacific: vertical distributions in the warm pool and in the high nutrient low chlorophyll conditions. Deep-Sea Res. 48: 297–314.CrossRefGoogle Scholar
  13. Bockstahler KR & Coats DW (1993) Grazing of the mixotrophic dinflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay. Mar. Biol. 116: 477–487.CrossRefGoogle Scholar
  14. Boenigk J (2000) Feeding mechanisms and the significance of food selection in heterotrophic nanoflagellates. University of Cologne (Germany), 133 pp.Google Scholar
  15. Boyd PW & Harrison PJ (1999) Canadian JGOFS in the NE Subarctic Pacific. Deep Sea Res. Part II. Top. Stud. Oceanogr. 46(11-12).Google Scholar
  16. Boyd PW, Whitney FA, Harrison PJ & Wong CS (1995) The NE subarctic Pacific in winter: ii. Biological rate processes. Mar. Ecol. Prog. Ser. 128: 11–24.CrossRefGoogle Scholar
  17. Brandt SM & Sleigh MA (2000) The quantitative occurrence of different taxa of heterotrophic flagellates in Southhampton Water, U.K. Estuar. Coast. Shelf Sci. 51: 91–102.CrossRefGoogle Scholar
  18. Buck KR, Nielsen TG, Hansen BW, Gastrup-Hansen D & Thomsen HA (1998) Infiltration phyto-and protozooplankton assemblages in the annual sea ice of Disko Island, West Greenland, spring 1996. Polar Biol. 20: 377–381.CrossRefGoogle Scholar
  19. Buck KR, Barry JP & Simpson AGB (2000) Monterey Bay cold seep biota: Euglenozoa with chemoautotrophic bacterial epibionts. Eur. J. Protistol. 36: 117–126.Google Scholar
  20. Burkill PH (Ed) (1999) ARABESQUE: UK JGOFS Process Study in the Arabian Sea. Deep Sea Res. Part II. Top. Stud. Oceanogr. 46(3-4).Google Scholar
  21. Burkill PH, Edwards ES & Sleigh MA (1995) Microzooplankton and their role in controlling phytoplankton growth in the marginal ice zone of the Bellingshausen Sea. Deep-Sea Res. 42: 1277–1290.CrossRefGoogle Scholar
  22. Calbet A (2001) Mesozooplankton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnol. Oceanogr. 46: 1824–1830.CrossRefGoogle Scholar
  23. Calbet A & Landry MR (1999) Mesozooplankton influences on the microbial food web: direct and indirect trophic interactions in the oligotrophic open ocean. Limnol. Oceanogr. 44: 1370–1380.CrossRefGoogle Scholar
  24. Campbell L, Nolla HA & Vaulot D (1994) The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnol. Oceanogr. 39: 954–961.CrossRefGoogle Scholar
  25. Capriulo GM (1990) Feeding-related ecology of marine protozoa. In Capriulo GM (Ed) Ecology of Marine Protozoa (pp 186–259). Oxford University Press, New York.Google Scholar
  26. Caron DA (2000) Symbiosis and mixotrophy among pelagic microorganisms. In Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 495–523). Wiley-Liss, New York.Google Scholar
  27. Caron DA & Goldman JC (1990) Protozoan nutrient regeneration. In Capriulo GM (Ed) Ecology of Marine Protozoa (pp 283–306). Oxford University Press, New York.Google Scholar
  28. Caron DA, Lim EL, Kunze H, Cosper EM & Anderson DM (1989) Trophic interactions between nano-and microzooplankton and the 'brown tide'. In Cosper EM, Bricelj VM & Carpenter EJ (Eds) Novel Phytoplankton Blooms (pp 265–294). Springer, Berlin.Google Scholar
  29. Caron DA, Lim EL, Dennett MR, Gast RJ & DeLong EF (1999) Molecular phylogenetic analysis of the heterotrophic chrysophyte genus Paraphysomonas (Chrysophyceae), and the design of rRNA targeted oligonucleotide probes for two species. J. Phycol. 35: 824–837.CrossRefGoogle Scholar
  30. Caron DA, Dennett MR, Lonsdale DJ, Moran DM & Shalapyonok L (2000) Microzooplankton herbivory in the Ross Sea, Antarctica. Deep-Sea Res. Part II 47: 3249–3272.CrossRefGoogle Scholar
  31. Chase Z & Price NM (1997) Metabolic consequences of iron defi-ciency in heterotrophic marine protozoa. Limnol. Oceanogr. 42: 1673–1684.CrossRefGoogle Scholar
  32. Cole JJ, Findlay S & Pace ML (1988) Bacterial production in fresh and salt water ecosystems: a cross system overview. Mar. Ecol. Prog. Ser. 43: 1–10.CrossRefGoogle Scholar
  33. Christaki U, Van Wambeke F & Dolan JR (1999) Nanoflagellates (mixotrophs, heterotrophs, and autotrophs) in the oligotrophic eastern Mediterranean: standing stocks, bacterivory and relationships with bacterial production. Mar. Ecol. Prog. Ser. 181: 297–307.CrossRefGoogle Scholar
  34. del Giorgio PA, Gasol JM, Mura P, Vaque D & Duarte CM (1996) Protozoan control of the proportion of metabolically act304 ive bacteria in coastal marine plankton. Limnol. Oceanogr. 41: 1169–1179.CrossRefGoogle Scholar
  35. Diez B, Pedrós-Alió C & Massana R (2001a) Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing. Appl. Environ. Microbiol. 67: 2932–2941.CrossRefPubMedGoogle Scholar
  36. Diez B, Pedrós-Alió C, Marsh TL & Massana R (2001b) Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Appl. Environ. Microbiol. 67: 2942–2951.CrossRefPubMedGoogle Scholar
  37. Dolan JR (1997) Phosphorus and ammonia excretion by planktonic protists. Mar. Geol. 139: 109–122.CrossRefGoogle Scholar
  38. Dolan JR, Gallegos CL & Miogis A (2000) Dilution effects on microzooplankton in dilution grazing experiments. Mar. Ecol. Prog. Ser. 200: 127–139.CrossRefGoogle Scholar
  39. Ducklow HW (1983) Production and the fate of bacteria in the oceans. Bioscience 33: 494–501.CrossRefGoogle Scholar
  40. Ducklow H (2000) Bacterial production and biomass in the oceans. In Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 85–120). Wiley-Liss, New York.Google Scholar
  41. Ducklow H, Purdie DA, Williams PJ le B & Davies JM (1986) Bacterioplankton: a sink for carbon in a coastal marine plankton community. Science 232: 865–867.PubMedCrossRefGoogle Scholar
  42. Dupuy C, Le Gall S, Hartmann HJ & Beret M (1999) Retention of ciliates and flagellates by the oyster Crassostrea gigas in Frech Atlantic coastal ponds: protists as a trophic link between bacterioplankton and benthic suspension-feeders. Mar. Ecol. Prog. Ser. 177: 165–175.CrossRefGoogle Scholar
  43. Dyer BD & Obar RA (1994) Tracing the History of Eukaryotic Cells. Columbia University Press, New York, 259 pp.Google Scholar
  44. Epstein SS (1997) Microbial food webs in marine sediments. I. Trophic interactions and grazing rates in two tidal flat communities. Microb. Ecol. 34: 188–198.CrossRefPubMedGoogle Scholar
  45. Fahnenstiel GL, McCormick MJ, Lang GA, Redalje DG, Lohrenz SE, Markowitz M, Wagoner B & Carrick HJ (1995) Taxon-specific growth and loss rates for dominant phytoplankton populations from the northern Gulf of Mexico. Mar. Ecol. Prog. Ser. 117: 229–239.CrossRefGoogle Scholar
  46. Fenchel T (1984) Suspended marine bacteria as a food source. In Fasham MJ (Ed), Energy and Materials in Marine Ecosystems (pp 301–315). Plenum, New York.Google Scholar
  47. Fenchel T (1987) Ecology of Protozoa: The Biology of Free-living Phagotrophic Protists. Science Tech./Springer, Berlin, 197 pp.Google Scholar
  48. Fenchel T & Blackburn N (1999) Motile chemosensory behavior of phagotrophic protists: mechanisms for and efficiency in congregating at food patches. Protist 150: 325–336.PubMedCrossRefGoogle Scholar
  49. Ferrier-Pages C, Karner M & Rassoulzadegan F (1998) Release of dissolved amino acids by flagellates and ciliates grazing on bacteria. Oceanol. Acta 21: 485–494.CrossRefGoogle Scholar
  50. Fessenden L & Cowles TJ (1994) Copepod predation on phagotrophic ciliates in Oregon coastal waters. Mar. Ecol. Prog. Ser. 107: 103–111.CrossRefGoogle Scholar
  51. Finlay, B (2001) Protozoa. In: Encyclopedia of Biodiversity, Volume 4. (pp 901–915). Academic Press, New York.Google Scholar
  52. Froneman PW & Balarin MG (1998) Structure and grazing impact of the protozooplankton community in the waters surrounding the Prince Edward Islands (Southern Ocean). Polar Biol. 20: 198–205.CrossRefGoogle Scholar
  53. Froneman P & Perissinotto R (1996) Microzooplankton grazing in the Southern Ocean: Implications for the carbon cycle. P.S.Z.N. I: Mar. Ecol. 17: 99–115.CrossRefGoogle Scholar
  54. Fukuda R, Ogawa H, Nagata T & Koike I (1998). Direct determination of carbon and nitrogen contents of natural bacterial assemblages in marine environments. Appl. Envir.Microbiol. 64: 3352–3358.Google Scholar
  55. Gallegos CL (1989) Microzooplankton grazing on phytoplankton in the Rhode River, Maryland: nonlinear feeding kinetics. Mar. Ecol. Prog. Ser. 57: 23–33.CrossRefGoogle Scholar
  56. Gaul W, Antia AN & Koeve W (1999) Microzooplankton grazing and nitrogen supply of phytoplankton growth in the temperate and subtropical northeast Atlantic. Mar. Ecol. Prog. Ser. 189: 93–104.CrossRefGoogle Scholar
  57. Gifford DJ (1988) Impact of grazing by microzooplankton in the Northwest Arm of Halifax Harbour, Nova Scotia. Mar. Ecol. Prog. Ser. 47: 249–258.CrossRefGoogle Scholar
  58. Gooday AJ & Lambshead PDJ (1989) Influence of seasonally deposited phytodetritus on benthic foraminiferal populations in the bathyal northeast Atlantic: the species response. Mar. Ecol. Prog. Ser. 58: 53–67.CrossRefGoogle Scholar
  59. Gonzalez J & Suttle CA (1993) Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar. Ecol. Prog. Ser. 94: 1–10.CrossRefGoogle Scholar
  60. Gonzalez J, Sherr EB & Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. Environ. Microbiol. 56: 583–589.PubMedGoogle Scholar
  61. Gonzalez J, Sherr EB & Sherr BF (1993a) Differential feeding by marine flagellates on growing vs starving bacteria, and on motile vs non-motile bacteria. Mar. Ecol. Prog. Ser. 102: 257–267.CrossRefGoogle Scholar
  62. Gonzalez J, Sherr BF & Sherr EB (1993b) Digestive enzyme activity as a quantitative measure of protistan grazing: the acid lysozyme assay for bacterivory. Mar. Ecol. Prog. Ser. 100: 197–206.CrossRefGoogle Scholar
  63. Gude H (1989) The role of grazing on bacteria in plankton succession, In: Sommer U (Ed) Plankton Ecology: Succession in Plankton Communities (pp 337–364). Brock/Springer, Berlin.Google Scholar
  64. Guillou L, Moon-van der Staay SY, Claustre H, Partensky F & Vaulot D (1999a) Diversity and abundance of Bolidophyceae (Heterokonta) in two oceanic regions. Appl. Environ. Microbiol. 65: 4528–4536.PubMedGoogle Scholar
  65. Guillou L, Chretiennot-Dinet M-J, Boulben S, Moon-van der Staay SY & Vaulot D (1999b) Symbiomonas scintillans gen. et sp. nov. and Picophagus flagellatus gen. et sp. nov. (Heterokonta): two new heterotrophic flagellates of picoplanktonic size. Protist 150: 383–398.PubMedCrossRefGoogle Scholar
  66. Hahn MW & Hofle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol. Ecol. 35: 113–121.CrossRefPubMedGoogle Scholar
  67. Hall JA, Barrett DP & James MR (1993) The importance of phytoflagellate, heterotrophic flagellate and ciliate grazing on bacteria and picophytoplankton sized prey in a coastal marine environment. J. Plankton Res. 15: 1075–1086.CrossRefGoogle Scholar
  68. Hammer A, Gruttner C & Schumann R (1999) The effect of electrostatic charge of food particles on capture efficiency by Oxyrrhis marina Dujardin (dinoflagellate). Protist 150: 375–382.PubMedCrossRefGoogle Scholar
  69. Hansen PJ (1991) Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagic food web. Mar. Ecol. Prog. Ser. 73: 253–261.CrossRefGoogle Scholar
  70. Hansen PJ (1998) Phagotrophic mechanisms and prey selection in mixotrophic flagellates. In: Anderson DM, Cembella AD & Hallegraeff GM (Eds) Physiological Ecology of Harmful Algal Blooms (pp 525-537). Springer, Berlin.Google Scholar
  71. Havskum H & Hansen AS (1997) Importance of pigmented and colourless nano-sized protists as grazers on nanoplankton in a phosphate-depleted Norwegian fjord and in enclosures. Mar. Ecol. Prog. Ser. 12: 139–151.Google Scholar
  72. Honedeveld BJM, Bak RPM & van Duyl FC (1992) Bacterivory by heterotrophic nanoflagellates in marine sediments measured by uptake of fluorescently labeled bacteria. Mar. Ecol. Prog. Ser. 89: 63–71.CrossRefGoogle Scholar
  73. Hwang S-J & Heath RT (1997) Bacterial productivity and protistan bacterivory in coastal and offshore communities of Lake Erie. Can. J. Fish. Aquat. Sci. 54: 788–799.CrossRefGoogle Scholar
  74. Jacobson DM & Anderson OR (1996) Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol. 32: 279–285.CrossRefGoogle Scholar
  75. James MR & Hall JR (1998) Microzooplankton in different water masses associated with the Subtropical Convergence round the South Island, New Zealand. Deep-Sea Res. 45: 1689–1707.CrossRefGoogle Scholar
  76. Jeong HJ (1994) Predation by the heterotrophic dinoflagellate Protoperidinium cf divergens on copepod eggs and early naupliar stages. Mar. Ecol. Prog. Ser. 114: 203–208.CrossRefGoogle Scholar
  77. Jeong HJ (1999) The ecological roles of heterotrophic dinoflagellates in marine planktonic community. J. Eukaryotic Microbiol. 46: 390–396.CrossRefGoogle Scholar
  78. Jeong HJ & Latz MI (1994) Growth and grazing rates of the heterotrophic dinoflagellate, Protoperidinium, on red tide dinoflagellates. Mar. Ecol. Prog. Ser. 106: 173–185.CrossRefGoogle Scholar
  79. Jeong HJ, Shim JH, Lee CW, Kim JS & Koh SM (1999a) Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J. Eukaryotic Microbiol. 46: 69–76.CrossRefGoogle Scholar
  80. Jeong HJ, Shim JH, Kim JS, Park JY, Lee CW & 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.CrossRefGoogle Scholar
  81. Jones HJ, Leadbeater BC & Green JC (1993) Mixotrophy in marine species of Chrysochromulina (Prymnesiophyceae) - ingestion and digestion of a small green flagellate. J. Mar. Biol. Assoc. UK 73: 283–296.CrossRefGoogle Scholar
  82. Jumars PA, Penry DL, Baross JA, Perry MJ & Frost BW (1989) Closing the microbial loop: dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep-Sea Res. 36: 483–495.CrossRefGoogle Scholar
  83. Jurgens K, Wickham SA, Rothhaupt KO & Santer B (1996) Feeding rates of macro-and microzooplankton on heterotrophic nanoflagellates. Limnol. Oceanogr. 41: 1833–1839.CrossRefGoogle Scholar
  84. Jurgens K, Pernthaler J, Schalla S & Amann R (1999) Morphological and compositional changes in a planktonic bacterial community in response to enhanced protozoan grazing. Appl. Environ. Microbiol. 65: 1241–1250.PubMedGoogle Scholar
  85. Jurgens K & Gude H (1994) The potential importance of grazing resistant bacteria in planktonic systems. Mar. Ecol. Prog. Ser. 112: 169–188.CrossRefGoogle Scholar
  86. Jurgens K & Simek K (2000) Functional response and particle size selection of Halteria cf. grandinella, a common freshwater oligotrichous ciliates. Aquat. Microb. Ecol. 22: 57–68.CrossRefGoogle Scholar
  87. Kamiyama T (1994) The impact of grazing by microzooplankton in northern Hiroshima Bay, the Seto Inland Sea, Japan. Mar. Biol. 119: 77–88.CrossRefGoogle Scholar
  88. Kamiyama T, Itakura S & Nagasaki K (2000) Changes in microbial loop components: effects of a harmful algal bloom formation and its decay. Aquat. Microb. Ecol. 21: 21–30.CrossRefGoogle Scholar
  89. Karpov SA, Kersanach R & Williams DM (1998) Ultrastructure and 18sRNA gene sequences of a small heterotrophic flagellate Siluania monomastiga gen. et sp. nov. (Bicosoecida). Eur. J. Protistol. 34: 415–425.Google Scholar
  90. Kemp PF (1988) Bacterivory by benthic ciliates: significance as a carbon resource and impact on sediment bacteria. Mar. Ecol. Prog. Ser. 36: 151–161.CrossRefGoogle Scholar
  91. Klaas C (1997) Microprotozooplankton distribution and grazing impact in the open waters of the Antarctic Circumpolar Current. Deep-Sea Res. II 44: 375–393.CrossRefGoogle Scholar
  92. Klein-Breteler WCM, Schogt N, Baas M, Schouten S & Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar. Biol. 135: 191–198.CrossRefGoogle Scholar
  93. Kleppel GS (1993) On the diets of calanoid copepods. Mar. Ecol. Prog. Ser. 99: 183–195.CrossRefGoogle Scholar
  94. Koeve W & Ducklow H (Eds) (2001) JGOFS Research in the North Atlantic Ocean: a decade of research, synthesis and modeling. Deep Sea Res. Part II: Top. Stud. Oceanogr. 48(10).Google Scholar
  95. Kolaczyk A & Wiackowski K (1997) Induced defence in the ciliate Euplotes octocarinatus is reduced when alternative prey are available to the predator. Acta Protozool. 36: 57–61.Google Scholar
  96. Kolber ZS, VanDover CL, Niederman RA & Falkowski PG (2000) Bacterial photosynthesis in surface waters of the open ocean. Nature 407: 177–179.CrossRefPubMedGoogle Scholar
  97. Koshikawa H, Harada S, Watanabe M, Sato K & Akehata K (1996) Relative contribution of bacterial and photosynthetic production to metazooplankton as carbon sources. J. Plankton Res. 18: 2269–2281.CrossRefGoogle Scholar
  98. Landry MR (1993). Estimating rates of growth and grazing mortality of phytoplankton by the dilution method. In Kemp PF, Sherr BF, Sherr EB & Cole JJ (Eds), Handbook of Methods in Aquatic Microbial Ecology (pp 715–722). Lewis Publishers, Boca Raton, FL.Google Scholar
  99. Landry MR, Brown SL, Campbell L, Constantinou J & Liu H (1998) Spatial patterns in phytoplankton growth and microzooplankton grazing in the Arabian Sea during monsoon forcing. Deep-Sea Res. II 45: 2353–2368.CrossRefGoogle Scholar
  100. Landry MR, Constantinou J, Latasa M, Brown SL, Bidigare RR & Ondrusek ME (2000) Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II). III. Dynamics of phytoplankton growth and microzooplankton grazing. Mar. Ecol. Prog. Ser. 201: 73–83.CrossRefGoogle Scholar
  101. Latasa M, Landry MR, Schluter L & Bidigare RR (1997) Pigment specific growth and grazing rates of phytoplankton in the central equatorial Pacific. Limnol. Oceanogr. 42: 289–298.CrossRefGoogle Scholar
  102. Lavrentyev PJ, WS Gardner & JR Johnson (1997) Cascading trophic effects on aquatic nitrification: experimental evidence and potential implications. Aquat. Microb. Ecol. 13: 161–175.CrossRefGoogle Scholar
  103. Laybourn-Parry J, Mell EM & Roberts EC (2000) Protozoan growth rates in Antarctic lakes. Polar Biol. 23: 445–451.CrossRefGoogle Scholar
  104. LeeWJ & Patterson DJ (1998) Diversity and geographic distribution of free-living heterotrophic flagellates - analysis by PRIMER. Protist 149: 229–244.CrossRefGoogle Scholar
  105. Legendre L & Le Fevre, J (1995) Microbial food webs and the export of biogenic carbon in oceans. Aquat. Microb. Ecol. 9: 69–77.CrossRefGoogle Scholar
  106. Legendre L & Rassoulzadegan F (1996) Food-web mediated export of biogenic carbon in oceans: hydrodynamic control. Mar. Ecol. Prog. Ser. 145: 179–193.CrossRefGoogle Scholar
  107. Lessard EJ & Murrell MC (1998) Microzooplankton herbivory and phytoplankton growth in the northwestern Sargasso Sea. Aquat. Microb. Ecol. 16: 176–188.CrossRefGoogle Scholar
  108. Li WKW (1998) Annual average abundance of heterotrophic bacteria and Synechococcus in surface ocean waters. Limnol. Oceanogr. 43: 1746–1753.CrossRefGoogle Scholar
  109. Lim EL, Caron DA & Dennett MR (1999) The ecology of Paraphysomonas imperforata based on studies employing oligonucleotide probe identification in coastal water samples and enrichment culture. Limnol. Oceanogr. 44: 37–51.CrossRefGoogle Scholar
  110. Liu H & Buskey EJ (1999) The exopolymer secretions (EPS) layer surrounding Aureoumbra lagunensis cells affects growth, grazing and behavior of protozoa. Limnol. Oceanogr. 45: 1187–1191.CrossRefGoogle Scholar
  111. Loret P, Le Gall S, Dupuy C, Blanchot J, Pastoureaud A, Delasalle B, Caisey X & Jonquieres G (2000) Heterotrophic protists as a trophic link between picocyanobacteria and the pearl oyster Pinctada margaritifera in the Takapoto lagoon (Tuamotu Archipelago, French Polynesia). Aquat. Microb. Ecol. 22: 215–226.CrossRefGoogle Scholar
  112. Maranger R, Bird DF & Price NM (1998) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature 396: 248–251.CrossRefGoogle Scholar
  113. Menden-Deuer S & Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol. Oceanogr. 45: 569–579.CrossRefGoogle Scholar
  114. Miller CB, Frost BW, Wheeler PA, Landry MR, Welschmeyer NA & Powell TM (1991) Ecological dynamics in the subarctic Pacific, a possibly iron-limited ecosystem. Limnol. Oceanogr. 36: 1600–1615.CrossRefGoogle Scholar
  115. Moloney CL (1992) Simulation studies of trophic flows and nutrient cycles in Benguela upwelling foodwebs. In: Payne AIL, Brink KH, Mann KH & Hilborn R (Eds) Benguela Trophic Functioning. South Africa J. Mar. Sci. 12: 457–476.Google Scholar
  116. Montagnes DJS & Weiss T (2000) Fluctuating temperatures affect growth and production rates of planktonic ciliates. Aquat. Microb. Ecol. 21: 97–102.CrossRefGoogle Scholar
  117. Moon-van der Staay SY, De Wachter R & Vaulot D (2001) Oceanic 18S rDNA sequences from picoplankton reveal new eukaryotic lineages. Nature 409: 607–610.CrossRefPubMedGoogle Scholar
  118. Murray JW (Ed) (1995 & 1996) A U.S. JGOFS Process Study in the Equatorial Pacific. Deep Sea Res. Part II: Top. Stud. Oceanogr. 42(2-3) & 43(4-6).Google Scholar
  119. Murrell MC & Hollibaugh JT (1998) Microzooplankton grazing in northern San Francisco Bay measured by the dilution method. Aquat. Microb. Ecol. 15: 53–63.CrossRefGoogle Scholar
  120. Murzov SA & Caron DA (1996) Sporadic high abundances of naked amoebae in the Black Sea plankton. Aquat. Microb. Ecol. 11: 161–169.CrossRefGoogle Scholar
  121. Nagata T (2000) Production mechanisms of dissolved organic matter. In Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 121–151). Wiley-Liss, New York.Google Scholar
  122. Nagata T & Kirchman DL (1990) Release of dissolved free and combined amino acids by bacterivorous marine flagellates. Limnol. Oceanogr. 36: 433–443.CrossRefGoogle Scholar
  123. Neuer S & Cowles TJ (1994) Protist herbivory in the Oregon upwelling system. Mar. Ecol. Prog. Ser. 113: 147–163.CrossRefGoogle Scholar
  124. Nodwell LM & Price NM (2001) Direct use of inorganic colloidal iron by marine mixotrophic phytoplankton. Limnol. Oceanogr. 46: 765–777.CrossRefGoogle Scholar
  125. Nygaard K & Tobiesen A (1993) Bacterivory in algae - a survival strategy during nutrient limitation. Limnol. Oceanogr. 38: 273–279.CrossRefGoogle Scholar
  126. Pace ML (1988) Bacterial mortality and the fate of bacterial production. Hydrobiologia 159: 41–49.Google Scholar
  127. Pace ML, McManus GB & Findlay SEG (1990) Planktonic community structure determines the fate of bacterial production in a temperate lake. Limnol. Oceanogr. 35: 795–808.CrossRefGoogle Scholar
  128. Palmisano AC & Garrison DL (1993) Microorganisms in Antarctic sea ice. Antarctic Microbiol. 1: 67–218.Google Scholar
  129. Partensky P, Hess WR & Vaulot D (1999) Prochlorococcus, amarine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63: 106–127.PubMedGoogle Scholar
  130. Pedros-Alio C, Calderon-Paz JI, MacLean MH, Medina G, Marrase C, Gasol JM & Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol. Ecol. 32: 143–155.PubMedGoogle Scholar
  131. Perez MT, Dolan JR & Fukai E (1997) Planktonic oligotrich ciliates in the NWMediterranean: growth rates and consumption by copepods. Mar. Ecol. Prog. Ser. 155: 89–101.CrossRefGoogle Scholar
  132. Pomeroy LR (1974) The ocean's food web: a changing paradigm. BioScience 24: 499–504.CrossRefGoogle Scholar
  133. Posch T, Simek K, Vrba J, Pernthaler J, Nedoma J, Sattler B, Sonntag B & Psenner R (1999) Predator-induced changes of bacterial size-structure and productivity studies on an experimental microbial community. Aquat. Microb. Ecol. 18: 235–246.CrossRefGoogle Scholar
  134. Putland J (2000) Microzooplankton herbivory and bacterivory in Newfoundland coastal waters during spring, summer and winter. J. Plankton Res. 22: 253–277.CrossRefGoogle Scholar
  135. Rasmussen LD, Hansen LH & Soerensen SJ (2001) Genetic diversity of kinetoplastide (protozoa) in natural environments revealed by denaturing gradient gel eletrophoresis. ISME-9 Abstract Mo.089, Amsterdam, August 2001.Google Scholar
  136. Reckermann M (1997) Trophic interactions between picophytoplankton and micro-and nanozooplankton in the western Arabian Sea during the NE monsoon 1993. Aquat. Microb. Ecol. 12: 263–273.CrossRefGoogle Scholar
  137. Rice J, Sleigh MA, Burkill PH, Tarran GA, O'Conner CD & Zubkov M (1997) Flow cytometric analysis of characteristics of hybridization of species-specific fluorescent oligonucleotide probes to rRNA of marine nanoflagellates. Appl. Environ. Microbiol. 63: 938–944.PubMedGoogle Scholar
  138. Rivkin RB & 18 others (1996) Vertical flux of biogenic carbon in the ocean: is there food web control? Science 272: 1163–1166.PubMedCrossRefGoogle Scholar
  139. Ruiz A, Franco K & Villate F. (1998) Microzooplankton grazing in the Estuary of Mundaka, Spain, and its impact on phytoplankton distribution along the salinity gradient. Aquat. Microb. Ecol. 14: 281–288.CrossRefGoogle Scholar
  140. Sakka A, Legendre, Gosselin M & Delesalle B (2000) Structure of the oligotrophic planktonic food web under low grazing of heterotrophic bacteria: Takapoto Atoll, French Polynesia. Mar. Ecol. Prog. Ser. 197: 1–17.CrossRefGoogle Scholar
  141. Sandberg J, Elmgren R & Wulff F (2000) Carbon flows in Baltic Sea food webs - a re-evaluation using a mass balance approach. J. Mar. Syst. 25: 249–260.CrossRefGoogle Scholar
  142. Sanders RW, Caron DA & Berninger UG (1992) Relationship between bacteria and heterotrophic nanoplankton in marine and fresh waters: an inter-ecosystem comparison. Mar. Ecol. Prog. Ser. 86: 1–14.CrossRefGoogle Scholar
  143. Sanders RW, Berninger UG, Lim EL, Kemp PF & Caron DA (2000) Heterotrophic and mixotrophic nanoplankton predation on picoplankton in the Sargasso Sea and on Georges Bank. Mar. Ecol. Prog. Ser. 192: 103–118.CrossRefGoogle Scholar
  144. Sautour B, Artigas LF, Delmas D, Herbland A & Laborde P (2000) Grazing impact of micro-and mesozooplankton during a spring situation in coastal waters off the Gironde estuary. J. Plankton Res. 22: 531–552.CrossRefGoogle Scholar
  145. Scott FJ, Davidson AT & Marchant HJ (2001) Grazing by the Antarctic sea ice ciliate Pseudocohnilembus. Polar Biol. 24: 127–131.CrossRefGoogle Scholar
  146. Sherr BF & Sherr EB (1991) Proportional distribution of total numbers, biovolume, and bacterivory among size classes of 2-20 (m nonpigmented marine flagellates. Mar. Microb. Food Webs 5: 227–237.Google Scholar
  147. Sherr EB & Sherr BF (1992). Trophic roles of pelagic protists: phagotrophic flagellates as herbivores. Arch. Hydrobiol. Beih. 37: 165–172.Google Scholar
  148. Sherr EB & Sherr BF (1994) Bacterivory and herbivory: key roles of phagotrophic protists in pelagic food webs. Microb. Ecol. 28: 223–235.CrossRefGoogle Scholar
  149. Sherr EB & Sherr BF (2002) Phagotrophy in aquatic microbial food webs. In: Newell S (Ed) Manual of Environmental Microbiology II (pp 409–418). ASM Press, Washington, DC.Google Scholar
  150. Sherr BF & Sherr EB (2000) Marine microbes: an overview. In: Kirchman D (Ed) Microbial Ecology of the Oceans (pp 13–46). Wiley-Liss, New York.Google Scholar
  151. Sherr BF, Sherr EB & Albright LJ (1987) Bacteria: link or sink? Science 235: 88–89.CrossRefGoogle Scholar
  152. Sherr BF, Sherr EB & Pedros-Alio C (1989) Simultaneous measurement of rates of bacterioplankton production and protozoan bacterivory in estuarine water. Mar. Ecol. Prog. Ser. 54: 209–219.CrossRefGoogle Scholar
  153. Sherr EB, Sherr BF, Hadas O & Berman T (1991a) High abundance of pico-plankton-ingesting ciliates during late fall in Lake Kinneret, Israel. J. Plankton Res. 13: 789–812.CrossRefGoogle Scholar
  154. Sherr EB, Sherr BF & McDaniel J (1991b) Clearance rates of <6 µm fluorescently labeled algae (FLA) by estuarine protozoa: potential grazing impact of flagellates and ciliates. Mar. Ecol. Prog. Ser. 69: 81–92.CrossRefGoogle Scholar
  155. Sherr BF, Sherr EB & McDaniel J (1992) Effect of protistan grazing on the frequency of dividing cells (FDC) in bacterioplankton assemblages. Appl. Environ. Microbiol. 58: 2381–2385.PubMedGoogle Scholar
  156. Sherr EB, Caron DA & Sherr BF (1993) Staining of heterotrophic protists for visualization via epifluorescence microscopy. In: Kemp P, Sherr B, Sherr E & Cole J (Eds) Current Methods in Aquatic Microbial Ecology (pp 213–228). Lewis, New York.Google Scholar
  157. Sherr EB, Sherr BF & Fessenden L (1997) Heterotrophic protists in the central Arctic Ocean. Deep-Sea Res. II 44: 1665–1682.CrossRefGoogle Scholar
  158. Sieburth JMcN (1981) Protozoan bacterivory in pelagic marine waters. In: Hobbie JE & Williams PleB (Eds) Heterotrophic Activity in the Sea, NATO Conference Series IV, Vol. 15, (pp 405-444).Google Scholar
  159. Sieburth JMcN & Davis PG (1982) The role of heterotrophic nanoplankton in the grazing and nurturing of planktonic bacteria in the Sargasso and Caribbean Seas. Ann. Inst. Oceanogr. Paris 58: 285–296.Google Scholar
  160. Simek K & Straskrabova K (1992) Bacterioplankton production and protozoan bacterivory in a mesotrophic reservoir. J. Plankton Res. 14: 773–788.CrossRefGoogle Scholar
  161. Simek K, Armengol J, Comerma M, Garcia JC, Chrzanowski TH, Kojecka P, Macek M, Nedoma J & Straskrabova V (1999) Impacts of protistan grazing on bacterial dynamics and composition in reservoirs of different trophy. In: Tundisi JG & Straskraba M (Eds) Theoretical Reservoir Ecology and its Applications (pp 267-282). Backhuys Publishers.Google Scholar
  162. Simon M, Bunte C, Schulz M, Weiss M & Wunsch C (1998) Bacterioplankton dynamics in Lake Constance (Bodensee): Substrate utilization, growth control, and long-term trends. Arch. Hydrobiol. Spec. Iss. Adv. Limnol. 53: 195–221.Google Scholar
  163. Sleigh MA & Zubkov MV (1998) Methods of estimating bacterivory by protozoa. Eur. J. Protistol.Google Scholar
  164. Smetacek V (1981) The annual cycle of protozooplankton in Kiel Bight. Mar. Biol. 63: 1–11.CrossRefGoogle Scholar
  165. Solic M & Krstulovic N (1994) Role of predation in controlling bacterial and heterotrophic nanoflagellate standing stocks in the coastal Adriatic Sea: seasonal patterns. Mar. Ecol. Prog. Ser. 114: 219–235.CrossRefGoogle Scholar
  166. Stelfox-Widdicombe CE, Edwards ES, Burkill PH & Sleigh MA (2000) Microzooplankton grazing activity in the temperate and sub-tropical NE Atlantic: summer 1996. Mar. Ecol. Prog. Ser. 208: 1–12.CrossRefGoogle Scholar
  167. Stoecker DK & Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J. Plankton Res. 12: 891–908.CrossRefGoogle Scholar
  168. Stone L & Berman T (1993) Positive feedback in aquatic ecosystems: the case of the microbial loop. Bull. Math. Biol. 55: 919–936.Google Scholar
  169. Straile D (1997) Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence on food concentration, predator-prey weight ratio, and taxonomic group. Limnol. Oceanogr. 42: 1375–1385.CrossRefGoogle Scholar
  170. Strom SL (1991) Growth and grazing rates of the herbivorous dinoflagellate Gymnodinium sp from the open subarctic Pacific Ocean. Mar. Ecol. Prog. Ser. 78(2): 103–113.CrossRefGoogle Scholar
  171. Strom SL (2000) Bacterivory: interactions between bacteria and their grazers. In: Kirchman DL (Ed) Microbial Ecology of the Oceans (pp 351–286). Wiley-Liss, New York.Google Scholar
  172. Strom SL & Morello TA (1998) Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J. Plankton Res. 20: 831–846.CrossRefGoogle Scholar
  173. Strom SL & Strom MW (1996) Microplankton growth, grazing, and community structure in the northern Gulf of Mexico. Mar. Ecol. Prog. Ser. 130: 229–240.CrossRefGoogle Scholar
  174. Strom SL, Postel JR & Booth BC (1993) Abundance, variability, and potential grazing impact of planktonic ciliates in the open subarctic Pacific Ocean. Prog. Oceanogr. 32: 185–203.CrossRefGoogle Scholar
  175. Strom SL, Benner R, Zeigler S & Dagg MJ (1997) Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol. Oceanogr. 36: 50–63.CrossRefGoogle Scholar
  176. Strom SL, Miller CB & Frost BW (2000) What sets lower limits to phytoplankton stocks in high-nitrate, low-chlorophyll regions of the open ocean? Mar. Ecol. Prog. Ser. 193: 19–31.CrossRefGoogle Scholar
  177. Strom SL, Brainard MA, Holms JL & Olson MB (2001) Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Mar. Biol. 138: 355–368.CrossRefGoogle Scholar
  178. Suzuki MT (1999) Effect of protistan bacterivory on coastal bacterioplankton diversity. Aquat. Microb. Ecol. 20: 261–272.CrossRefGoogle Scholar
  179. Swanberg NR & Caron DA (1991) Patterns of sarcodine feeding in epipelagic oceanic plankton. J. Plankton Res. 13: 287–312.CrossRefGoogle Scholar
  180. Tamigneaux E, Mingelbier M, Klein B & Legendre L (1997) Grazing by protists and seasonal changes in the size structure of protozooplankton and phytoplankton in a temperate nearshore environment (western Gulf of St. Lawrence, Canada). Mar. Ecol. Prog. Ser. 146: 231–247.CrossRefGoogle Scholar
  181. Tett P & Wilson H (2000) From biogeochemical to ecological models of marine microplankton. J. Mar. Syst. 25: 431–446.CrossRefGoogle Scholar
  182. Thingstad TF, Hagstrom A & Rassoulzadegan F (1997) Accumulation of degradable DOC in surface waters: is it caused by a malfunctioning microbial loop? Limnol. Oceanogr. 42: 398–404.CrossRefGoogle Scholar
  183. Thingstad TF, Perez M, Pelegri S, Dolan J & Rassoulzadegan F (1999) Trophic control of bacterial growth in microcosms containing a natural community from northwest Mediterranean surface waters. Aquat. Microb. Ecol. 18: 145–156.CrossRefGoogle Scholar
  184. Tong SM, Nygaard K, Bernard C, Vors N & Patterson DJ (1998) Heterotrophic flagellates from the water column in Port Jackson, Sydney, Australia. Eur. J. Protistology 34: 162–194.Google Scholar
  185. Tranvik LJ, Sherr EB & Sherr BF (1993) Uptake and utilization of 'colloidal DOM' by heterotrophic flagellates in seawater. Mar. Ecol. Prog. Ser. 92: 301–309.CrossRefGoogle Scholar
  186. Turley CM & Carstens M (1991) Pressure tolerance of oceanic flagellates: implications for remineralization of organic matter. Deep-Sea Res. 38: 403–413.CrossRefGoogle Scholar
  187. Van Hannen EJ, Veninga M, Bloem J, Gons HJ & Laanbroek HJ (1999) Genetic changes in bacterial community structure associated with protistan grazers. Arch. Hydrobiol. 145: 25–38.Google Scholar
  188. Vaque D, Gasol JM & Marrase C (1994) Grazing rates on bacteria: the significance of methodology and ecological factors. Mar. Ecol. Prog. Ser. 109: 263–274.CrossRefGoogle Scholar
  189. Verity PG (1991a) Feeding in planktonic protozoans: evidence for non-random acquisition of prey. Mar. Microb. Food Webs 5: 69–76.Google Scholar
  190. Verity PG (1991b) Measurement and simulation of prey uptake by marine planktonic ciliates fed plastidic and aplastidic nanoplankton. Limnol. Oceanogr. 36: 729–750.CrossRefGoogle Scholar
  191. Verity PG & Paffenhofer G-A (1996) On asssessment of prey ingestion by copepods. J. Plankton Res. 18: 1767–1779.CrossRefGoogle Scholar
  192. Verity PG & Vernet M (1992) Microzooplankton grazing, pigments, and composition of plankton communities during late spring in two Norwegian fjords. Sarsia 77: 263–274.Google Scholar
  193. Verity PG, Stoecker DK, Sieracki ME & Nelson JR (1993) Grazing, growth, and mortality of microzooplankton during the 1989 North Atlantic spring bloom at 470N, 180W. Deep-Sea Res. 40: 1793–1814.CrossRefGoogle Scholar
  194. Verity PG, Stoecker DK, Sieracki ME & Nelson JR (1996) Microzooplankton grazing of primary production at 1400W in the equatorial Pacific. Deep-Sea Res. 43: 1227–1255.CrossRefGoogle Scholar
  195. Vickerman K (1998) Revolution among the Protozoa, In: Coombs GH, Vickerman K, Sleigh MA & Warren A (Eds) Evolutionary Relationships among Protozoa (pp 1–24). Kluwer Academic Publishers, London.Google Scholar
  196. Vors N (1992a) Heterotrophic amoeba, flagellates and heliozoa from the Tvarminne area, Gulf of Finland, in 1988-1990. Ophelia 36: 1–109.Google Scholar
  197. Vors N (1992b) Ultrastructure and autecology of the marine, heterotrophic flagellates Leucocryptos marina (Braarud) Butcher 1967 (Katablepharidaceae/Kathabelpharidae) with a discussion of the genera Leucocryptos and Katablepharis/Kathabelpharis. Eur. J. Protistol. 28: 369–389.Google Scholar
  198. Waterhouse TY & Welschmeyer (1995) Taxon-specific analysis of microzooplankton grazing rates and phytoplankton growth rates. Limnol. Oceanogr. 40: 827–834.CrossRefGoogle Scholar
  199. Wallberg P, Johnson PR & Johnstone R (1999) Abundance, biomass and growth rates of pelagic microorganisms in a tropical coastal ecosystem. Aquat. Microb. Ecol. 18: 175–185.CrossRefGoogle Scholar
  200. Weisse T (1997) Growth and production of heterotrophic nanoflagellates in a meso-eutrophic lake. J. Plankton Res. 19: 703–723.CrossRefGoogle Scholar
  201. Weisse T (this volume) The significance of inter-and intraspecific variation in bacterivorous and herbivorous protists. Antonie van Leeuwenhoek, submitted.Google Scholar
  202. Weisse T & Muller H (1998) Planktonic protozoa and the microbial food web in Lake Constance. Arch. Hydrobiol. Spec. Iss. Adv. Limnol. 53: 223–254.Google Scholar
  203. Welschmeyer N, Goericke R, Strom S & Peterson W (1991) Phytoplankton growth and herbivory in the subarctic Pacific: A chemotaxonomic analysis. Limnol. Oceanogr. 36: 1631–1649.CrossRefGoogle Scholar
  204. Wicklow BJ (1997) Signal-induced defensive phenotypic changes in ciliated protists: morphological and ecological implications for predator and prey. J. Eukaryotic Microbiol. 44: 176–188.CrossRefGoogle Scholar
  205. Wolfe GV (2000) The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol. Bull. 198: 225–244.PubMedCrossRefGoogle Scholar
  206. Wolfe GV, Steinke M & Kirst GO (1997) Grazing activated chemical defense in a unicellular marine alga. Nature 387: 894–897.CrossRefGoogle Scholar
  207. Zubkov MV, Sleigh MA & Burkill PH (1998) Measurement of bacterivory by protists in open ocean waters. FEMS Microb. Ecol. 27: 85–102.CrossRefGoogle Scholar
  208. Zubkov MV, Sleigh MA & Burkill PH (2000) Assaying picoplankton by flow cytometry of underway samples collected along a meridional transect across the Atlantic Ocean. Aquat. Microb. Ecol. 21: 13–20.CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.College of Oceanic and Atmospheric SciencesOregon State UniversityCorvallisUSA

Personalised recommendations