Skip to main content
SpringerLink
Log in

Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea

Hydrobiologia Aims and scope Submit manuscript

Cite this article

Abstract

Understanding the processes that regulate phytoplankton biomass and growth rate remains one of the central issues for biological oceanography. While the role of resources in phytoplankton regulation (`bottom up' control) has been explored extensively, the role of grazing (`top down' control) is less well understood. This paper seeks to apply the approach pioneered by Frost and others, i.e. exploring consequences of individual grazer behavior for whole ecosystems, to questions about microzooplankton–phytoplankton interactions. Given the diversity and paucity of phytoplankton prey in much of the sea, there should be strong pressure for microzooplankton, the primary grazers of most phytoplankton, to evolve strategies that maximize prey encounter and utilization while allowing for survival in times of scarcity. These strategies include higher grazing rates on faster-growing phytoplankton cells, the direct use of light for enhancement of protist digestion rates, nutritional plasticity, rapid population growth combined with formation of resting stages, and defenses against predatory zooplankton. Most of these phenomena should increase community-level coupling (i.e. the degree of instantaneous and time-dependent similarity) between rates of phytoplankton growth and microzooplankton grazing, tending to stabilize planktonic ecosystems. Conversely, phytoplankton, whose mortality in the sea is overwhelmingly due to microzooplankton grazing, should experience strong pressure to evolve grazing resistence. Strategies may include chemical, morphological, and `nutrient deficit' defenses. Successful deployment of these defenses should lead to uncoupling between rates of phytoplankton growth and microzooplankton grazing, promoting instability in ecosystem structure. Understanding the comparative ecosystem dynamics of various ocean regions will require an appreciation of how protist grazer behavior and physiology influence the coupling between rates of phytoplankton growth and microzooplankton grazing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Andersson, A., U. Larsson & Å. Hagström, 1986. Size-selective grazing by a microflagellate on pelagic bacteria. Mar. Ecol. Prog. Ser. 33: 51-57.

    Google Scholar 

  • Atkinson, A., 1996. Subantarctic copepods in an oceanic, low chlorophyll environment: ciliate predation, food selectivity and impact on prey populations. Mar. Ecol. Prog. Ser. 130: 85-96.

    Google Scholar 

  • Banse, K., 1992. Grazing, temporal changes of phytoplankton concentrations, and the microbial loop in the open sea. In Falkowski, P. G. & A. D. Woodhead (eds), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum, New York: 409-440.

    Google Scholar 

  • Bernard, C. & F. Rassoulzadegan, 1993. The role of picoplankton (cyanobacteria and plastidic picoflagellates) in the diet of tintinnids. J. Plankton Res. 15: 361-373.

    Google Scholar 

  • Boenigk, J., C. Matz, K. Jurgens & H. Arndt, 2001a. The influence of preculture conditions and food quality on the ingestion and digestion process of three species of heterotrophic nanoflagellates. Microb. Ecol. 42: 168-176.

    Google Scholar 

  • Boenigk, J., C. Matz, K. Jürgens & H. Arndt, 2001b. Confusing selective feeding with differential digestion in bacterivorous nanoflagellates. J. Eukaryot. Microbiol. 48: 425-432.

    Google Scholar 

  • Boyd, P.W., In press. The role of iron in the biogeochemistry of the Southern Ocean and Equatorial Pacific: a comparison of in situ iron enrichments. Deep-Sea Res. II.

  • Broglio, E., M. Johansson & P. R. Jonsson, 2001. Trophic interaction between copepods and ciliates: effects of prey swimming behavior on predation risk. Mar. Ecol. Prog. Ser. 220: 179-186.

    Google Scholar 

  • Burkill, P. H., E. S. Edwards, A. W. G. John & M. A. Sleigh, 1993. Microzooplankton and their herbivorous activity in the northeastern Atlantic Ocean. Deep-Sea Res. II 40: 479-493.

    Google Scholar 

  • Burkill, P. H., R. F. C. Mantoura, C. A. Llewellyn & N. J. P. Owens, 1987. Microzooplankton grazing and selectivity of phytoplankton in coastal waters. Mar. Biol. 93: 581-590.

    Google Scholar 

  • Buskey, E. J., 1997. Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum. Mar. Ecol. Prog. Ser. 153: 77-89.

    Google Scholar 

  • Buskey, E. J. & C. J. Hyatt, 1995. Effects of the Texas (U.S.A.) ‘brown tide’ alga on planktonic grazers. Mar. Ecol. Prog. Ser. 126: 285-292.

    Google Scholar 

  • Buskey, E., L. Mills & E. Swift, 1983. The effects of dinoflagellate bioluminescence on the swimming behavior of a marine copepod. Limnol. Oceanogr. 28: 575-579.

    Google Scholar 

  • Butler, N. M., C. A. Suttle & W. E. Neill, 1989. Discrimination by freshwater zooplankton between single algal cells differing in nutritional status. Oecologica 78: 368-372.

    Google Scholar 

  • Calado, A. J., S. C. Craveiro & O. Moestrup, 1998. Taxonomy and ultrastructure of a freshwater, heterotrophic Amphidinium (Dinophyceae) that feeds on unicellular protists. J. Phycol. 34: 536-554.

    Google Scholar 

  • Calbet, A., M. R. Landry & S. Nunnery, 2001. Bacteria-flagellate interactions in the microbial food web of the oligotrophic subtropical North Pacific. Aquat. Microb. Ecol. 23: 283-292.

    Google Scholar 

  • Capriulo, G. M. & E. J. Carpenter, 1980. Grazing by 35–202 µm micro-zooplankton in Long Island Sound. Mar. Biol. 56: 319-326.

    Google Scholar 

  • Capriulo, G.M., K. Gold & A. Okubo, 1982. Evolution of the lorica in tintinnids: a possible selective advantage. Ann. Inst. oceanogr. 58: 319-324.

    Google Scholar 

  • Caron, D. A., 2000. Symbiosis and mixotrophy among pelagic microorganisms. In Kirchman, D. A. (ed.), Microbial Ecology of the Oceans. John Wiley and Sons, New York: 495-523.

    Google Scholar 

  • Caron, D. A., J. C. Goldman & T. Fenchel, 1990. Protozoan respiration and metabolism. In Capriulo, G. M. (ed.), Ecology of Marine Protozoa. Oxford University Press, New York: 307-322.

    Google Scholar 

  • Carrias, J.-F., A. Thouvenot, C. Amblard & T. Sime-Ngando, 2001. Dynamics and growth estimates of planktonic protists during early spring in Lake Pavin, France. Aquat. Microb. Ecol. 24: 163-174.

    Google Scholar 

  • Chesson, J., 1983. The estimation and analysis of preference and its relationship to foraging models. Ecology 64: 1297-1304.

    Google Scholar 

  • Cowles, T. J., R. J. Olson & S.W. Chishom, 1988. Food selection by copepods: discrimination on the basis of food quality. Mar. Biol. 100: 41-49.

    Google Scholar 

  • del Giorgio, P. A., J. M. Gasol, D. Vaqué, P. Mura, S. Agustí & C.M. Duarte, 1996. Bacterioplankton community structure: Protists control net production and the proportion of active bacteria in a coastal marine community. Limnol. Oceanogr. 41: 1169-1179.

    Google Scholar 

  • DeMott, W. R., 1995. The influence of prey hardness on Daphnia's selectivity for large prey. Hydrobiologia 307: 127-138.

    Google Scholar 

  • Dolan, J. R., 1991. Guilds of ciliate microzooplankton in the Chesapeake Bay. Estuar. coast. shelf Sci. 33: 137-152.

    Google Scholar 

  • Dolan, J. R., C. L. Gallegos & A. Moigis, 2000. Dilution effects on microzooplankton in dilution grazing experiments. Mar. Ecol. Prog. Ser. 200: 127-139.

    Google Scholar 

  • Droop, M. R., 1966. The role of algae in the nutrition of Heteramoeba clara Droop, with notes on Oxyrrhis marina Dujardin and Philodina roseola Ehrenberg. In Barnes, H. (ed.), Some Contemporary Studies in Marine Science. G. Allen and Unwin Ltd., London: 269-282.

    Google Scholar 

  • Edwards, A. M. & A. Yool, 2000. The role of higher predation in plankton population models. J. Plankton Res. 22: 1085-1112.

    Google Scholar 

  • Fasham, M. J. R., H. W. Ducklow & S. M. McKelvie, 1990. A nitrogen-based model of plankton dynamics in the oceanic mixed layer. J. mar. Res. 48: 591-639.

    Google Scholar 

  • Fenchel, T., 1987. Ecology of protozoa. Science Tech., Madison: 197 pp.

    Google Scholar 

  • Fessenden, L. & T. J. Cowles, 1994. Copepod predation on phagotrophic ciliates in Oregon coastal waters. Mar. Ecol. Prog. Ser. 107: 103-111.

    Google Scholar 

  • Finlay, B. J., 1983. Influence of physiological state on indices of respiration rate in protozoa. Comp. Biochem. Physiol. 74A: 211-219.

    Google Scholar 

  • Frost, B. W., 1972. Effects of size and concentration of food particles on the feeding behavior of the marine planktonic copepod Calanus pacificus. Limnol. Oceanogr. 17: 805-815.

    Google Scholar 

  • Frost, B. W., 1975. A threshold feeding behavior in Calanus pacificus. Limnol. Oceanogr. 20: 263-266.

    Google Scholar 

  • Frost, B. W., 1980. Grazing. In Morris, I. (ed.), The Physiological Ecology of Phytoplankton. University of California Press, Berkeley: 465-491.

    Google Scholar 

  • Frost, B. W., 1987. Grazing control of phytoplankton stock in the open subarctic Pacific Ocean: a model assessing the role of mesozooplankton, particularly the large calanoid copepods Neocalanus spp. Mar. Ecol. Prog. Ser. 39: 49-68.

    Google Scholar 

  • Frost, B. W., 1991. The role of grazing in nutrient-rich areas of the open sea. Limnol. Oceanogr. 36: 1616-1630.

    Google Scholar 

  • Frost, B.W., 1993. A modelling study of processes regulating plankton standing stock and production in the open subarctic Pacific Ocean. Prog. Oceanogr. 32: 17-56.

    Google Scholar 

  • Frost, B. W. & N. C. Franzen, 1992. Grazing and iron limitation in the control of phytoplankton stock and nutrient concentration: a chemostat analogue of the Pacific equatorial upwelling zone. Mar. Ecol. Prog. Ser. 83: 291-303.

    Google Scholar 

  • Gall, M. P., P. W. Boyd, J. Hall, K. A. Safi & H. Chang, 2001. Phytoplankton processes. Part 1: community structure during the Southern Ocean iron RElease Experiment (SOIREE). Deep-Sea Res. II 48: 2551-2570.

    Google Scholar 

  • Gifford, D. J., 1993. Protozoa in the diets of Neocalanus spp. in the oceanic subarctic Pacific Ocean. Prog. Oceanogr. 32: 223-237.

    Google Scholar 

  • Goldman, J. C. & M. R. Dennett, 1990. Dynamics of prey selection by an omnivorous flagellate. Mar. Ecol. Prog. Ser. 59: 183-194.

    Google Scholar 

  • Goldman, J. C., J. J. McCarthy & D. G. Peavey, 1979. Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279: 210-215.

    Google Scholar 

  • Gonzalez, J. M., 1996. Efficient size-selective bacterivory by phagotrophic nanoflagellates in aquatic systems. Mar. Biol. 126: 785-789.

    Google Scholar 

  • Gonzalez, J. M.& C. A. Suttle, 1993. Grazing by marine nanoflagellates on viruses and virus-sized particles: ingestion and digestion. Mar. Ecol. Prog. Ser. 94: 1-16.

    Google Scholar 

  • Gonzalez, J. M., E. B. Sherr & B. F. Sherr, 1990. Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl. envir. Microbiol. 56: 583-589.

    Google Scholar 

  • Gonzalez, J. M., E. B. Sherr & B. F. Sherr, 1993. Differential feeding by marine flagellates on growing vs. starving, and on motile vs. non-motile, bacterial prey. Mar. Ecol. Prog. Ser. 102: 257-267.

    Google Scholar 

  • Halliwell, B. & J. M. C. Gutteridge, 1989. Free Radicals in Biology and Medicine, 2nd edn. Clarendon Press, Oxford: 543 pp.

    Google Scholar 

  • Hansen, B., P. K. Bjornsen & P. J. Hansen, 1994. The size ratio between planktonic predators and their prey. Limnol. Oceanogr. 39: 395-403.

    Google Scholar 

  • Hansen, P. J. & A. J. Calado, 1999. Phagotrophic mechanisms and prey selection in free-living dinoflagellates. J. Eukaryot. Microbiol. 46: 382-389.

    Google Scholar 

  • Hansen, P. J., P. K. Bjornsen & B. W. Hansen, 1997. Zooplankton grazing and growth: scaling within the 2–2000-µm body size range. Limnol. Oceanogr. 42: 687-704.

    Google Scholar 

  • Harvey, H.W., L. H. N. Cooper, M. V. Lebour & F. S. Russell, 1935. Plankton production and its control. J. mar. biol. Ass. U.K. 20: 407-441.

    Google Scholar 

  • Hay, M. E. & W. Fenical, 1988. Marine plant-herbivore interactions: the ecology of chemical defense. Ann. Rev. Ecol. Syst. 19: 111-145.

    Google Scholar 

  • Hutson, V., 1984. Predator mediated coexistence with a switching predator. Math. Biosci. 68: 233-246.

    Google Scholar 

  • Jacobson, D. M. & D. M. Anderson, 1996. Widespread phagocytosis of ciliates and other protists by marine mixotrophic and heterotrophic thecate dinoflagellates. J. Phycol. 32: 279-285.

    Google Scholar 

  • Jakobsen, H. H. & P. J. Hansen, 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.

    Google Scholar 

  • Jeong, H. J. & M. I. Latz, 1994. Growth and grazing rates of the heterotrophic dinoflagellates Protoperidinium spp. on red tide dinoflagellates. Mar. Ecol. Prog. Ser. 106: 173-185.

    Google Scholar 

  • Jeong, H. J., J. H. Shim, J. S. Kim, J. Y. Park, C. W. Lee & Y. Lee, 1999a. Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates. Mar. Ecol. Prog. Ser. 176: 263-277.

    Google Scholar 

  • Jeong, H. J., J. H. Shim, C. W. Lee, J. S. Kim & S. M. Koh, 1999b. Growth and grazing rates of the marine planktonic ciliate Strombidinopsis sp. on red-tide and toxic dinoflagellates. J. Euk. Microbiol. 46: 69-76.

    Google Scholar 

  • Johannes, R. E., 1964. Phosphorus excretion and body size in marine animals: microzooplankton and nutrient regeneration. Science 146: 923-924.

    Google Scholar 

  • Jonasdottir, S. H. and others 1998. Role of diatoms in copepod egg production: good, harmless or toxic? Mar. Ecol. Prog. Ser. 172: 305-308.

    Google Scholar 

  • Jones, R. I., 1994. Mixotrophy in planktonic protists as a spectrum of nutritional strategies. Mar. Microbial Food Webs 8: 87-96.

    Google Scholar 

  • Jonsson, P. R. & P. Tiselius, 1990. Feeding behaviour, prey detection and capture efficiency of the copepod Acartia tonsa feeding on planktonic ciliates. Mar. Ecol. Prog. Ser. 60: 35-44.

    Google Scholar 

  • Jürgens, K. & W. R. DeMott, 1995. Behavioral flexibility in prey selection by bacterivorous nanoflagellates. Limnol. Oceanogr. 40: 1503-1507.

    Google Scholar 

  • Kamiyama, T., 1997. Growth and grazing responses of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsa circularisquama. Mar. Biol. 128: 509-515.

    Google Scholar 

  • Keller, M. D., 1988/1989. Dimethyl sulfide production and marine phytoplankton: the importance of species composition and cell size. Biological Oceanogr. 6: 375-382.

    Google Scholar 

  • Keller, M. D., W. K. Bellows & R. R. L. Guillard, 1989. Dimethyl sulfide production in marine phytoplankton. In Saltzman, E. S. & W. J. Cooper (eds), Biogenic Sulfur in the Environment. American Chemical Society, Washington, DC: 167-183.

    Google Scholar 

  • Kuhlmann, H.-W., J. Kusch & K. Heckmann, 1999. Predatorinduced defenses in ciliated protozoa. In Tollrian, R. & C. D. Harvell (eds), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton: 142-159.

    Google Scholar 

  • Lam, R. K. & B. W. Frost, 1976. Model of copepod filtering response to changes in size and concentration of food. Limnol. Oceanogr. 21: 490-500.

    Google Scholar 

  • Landry, M. R., 1994. Methods and controls for measuring the grazing impact of planktonic protists. Mar. Microb. Food Webs 8: 37-57.

    Google Scholar 

  • Landry, M. R. & R. P. Hassett, 1982. Estimating the grazing impact of marine micro-zooplankton. Mar. Biol. 67: 283-288.

    Google Scholar 

  • Landry, M. R. and others 1997. Iron and grazing constraints on primary production in the central equatorial Pacific: an EqPac synthesis. Limnol. Oceanogr. 42: 405-418.

    Google Scholar 

  • Landry, M. R., J. Constantinou, M. Latasa, S. L. Brown, R. R. Bidigare & M. E. Ondrusek, 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: 57-72.

    Google Scholar 

  • Liu, H. & E. J. Buskey, 2000. The exopolymer secretions (EPS) layer surrounding Aureoumbra lagunensis cells affects growth, grazing, and behavior of protozoa. Limnol. Oceanogr. 45: 1187-1191.

    Google Scholar 

  • Longhurst, A., 1998. Ecological Geography of the Sea. Academic, San Diego: 398 pp.

    Google Scholar 

  • Loukos, H., B. Frost, D. E. Harrison & J. W. Murray, 1997. An ecosystem model with iron limitation of primary produciton in the equatorial Pacific at 140∘ W. Deep-Sea Res. II 44: 2221-2249.

    Google Scholar 

  • Mann, E. L. & S. W. Chisholm, 2000. Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific. Limnol. Oceanogr. 45: 1067-1076.

    Google Scholar 

  • Margalef, R., 1978. Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanol. Acta. 1: 493-509.

    Google Scholar 

  • May, R. M., 1977. Predators that switch. Nature 269: 103-104.

    Google Scholar 

  • May, R. M., 2001. Stability and Complexity in Model Ecosystems, 3rd edn. Princeton University Press, Princeton: 265 pp.

    Google Scholar 

  • McManus, G. B. & M. C. Ederington-Cantrell, 1992. Phytoplankton pigments and growth rates, and microzooplankton grazing in a large temperate estuary. Mar. Ecol. Prog. Ser. 87: 77-85.

    Google Scholar 

  • Miller, C. B., 1993. Pelagic production processes in the Subarctic Pacific. Prog. Oceanog. 32: 1-15.

    Google Scholar 

  • Miller, C. B., B. W. Frost, P. A. Wheeler, M. R. Landry, N. Welschmeyer & T. M. Powell, 1991. Ecological dynamics in the subarctic Pacific, a possibly iron-limited ecosystem. Limnol. Oceanogr. 36: 1600-1615.

    Google Scholar 

  • Miyake, A., T. Harumoto, B. Salvi & V. Rivola, 1990. Defensive function of pigment granules in Blepharisma japonicum. J. Eur. Protistol. 25: 310-315.

    Google Scholar 

  • Monger, B. C., M. R. Landry & S. L. Brown, 1999. Feeding selection of heterotrophic marine nanoflagellates based on the surface hydrophobicity of their picoplankton prey. Limnol. Oceanogr. 44: 1917-1927.

    Google Scholar 

  • Montagnes, D. J. S., 1996. Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium. Mar. Ecol. Prog. Ser. 130: 241-254.

    Google Scholar 

  • Murdoch, W.W., 1969. Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol. Monogr. 39: 335-354.

    Google Scholar 

  • Neuer, S. & T. J. Cowles, 1994. Protist herbivory in the Oregon upwelling system. Mar. Ecol. Prog. Ser. 113: 147-162.

    Google Scholar 

  • Oaten, A. & W.W. Murdoch, 1975. Switching, functional response, and stability in predator—prey systems. Am. Nat. 109: 299-318.

    Google Scholar 

  • Paffenhöfer, G.-A., 1998. Heterotrophic protozoa and small metazoa: feeding rates and prey-consumer interactions. J. Plankton Res. 20: 121-133.

    Google Scholar 

  • Pfiester, L. A. & D. M. Anderson, 1987. Dinoflagellate reproduction. In Taylor, F. J. R. (ed.), The Biology of Dinoflagellates. Blackwell Scientific, Oxford: 611-648.

    Google Scholar 

  • Pimm, S. L., 1984. The complexity and stability of ecosystems. Nature 307: 321-326.

    Google Scholar 

  • Pitchford, J. W. & J. Brindley, 1999. Iron limitation, grazing pressure and oceanic high nutrient—low chlorophyll (HNLC) regions. J. Plankton Res. 21: 525-547.

    Google Scholar 

  • Pomeroy, L. R., 1974. The ocean's food web, a changing paradigm. Bioscience 24: 499-504.

    Google Scholar 

  • Reid, P. C., 1987. Mass encystment of a planktonic oligotrich ciliate. Mar. Biol. 95: 221-230.

    Google Scholar 

  • Riemann, B., H. Havskum, F. Thingstad & C. Bernard, 1995. The role of mixotrophy in pelagic environments. NATOASI Ser. Mol. Ecol. Aquat. Microbes 38: 89-114.

    Google Scholar 

  • Riley, G. A., 1946. Factors controlling phytoplankton populations on Georges Bank. J. mar. Res. 6: 54-73.

    Google Scholar 

  • Royall, J. A. & H. Ischirpoulos, 1993. Evaluation of 2′,7′-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch. Biochem. Biophys. 302: 348-355.

    Google Scholar 

  • Sherr, E. B. & B. F. Sherr, Submitted. Significance of predation by protists in aquatic microbial food webs. Antonie van Leewenhoek ISME-9 Symposium Vol.

  • Sibbald, M. J., L. J. Albright & P. R. Sibbald, 1987. Chemosensory responses of a heterotrophic microflagellate to bacteria and several nitrogen compounds. Mar. Ecol. Prog. Ser. 36: 201-204.

    Google Scholar 

  • Skovgaard, A., 1998. Role of chloroplast retention in a marine dinoflagellate. Aquat. Microb. Ecol. 15: 293-301.

    Google Scholar 

  • Smayda, T. J., 1997. Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnol. Oceanogr. 42: 1137-1153.

    Google Scholar 

  • Spencer, K. C. (ed.), 1988. Chemical Mediation of Coevolution. Academic, San Diego: 609 pp.

    Google Scholar 

  • Spero, H. J., 1985. Chemosensory capabilities in the phagotrophic dinoflagellate Gymnodinium fungiforme. J. Phycol. 21: 181-184.

    Google Scholar 

  • Steele, J. H. & B. W. Frost, 1977. The structure of plankton communities. Phil. Trans. r. Soc. (B) 280: 485-534.

    Google Scholar 

  • Steele, J. H. & E. W. Henderson, 1992. The role of predation in plankton models. J. Plankton Res. 14: 157-172.

    Google Scholar 

  • Steinke, M., G. V. Wolfe & G. O. Kirst, 1998. Partial characterization of dimethylsulfoniopropionate (DMSP) lyase isozymes in 6 strains of Emiliania huxleyi. Mar. Ecol. Prog. Ser. 175: 215-225.

    Google Scholar 

  • Stephens, D. W. & J. R. Krebs, 1986. Foraging Theory. Princeton Univ., Princeton: 247 pp.

    Google Scholar 

  • Sterner, R.W. & R. F. Smith, 1993. Clearance, ingestion and release of N and P by Daphnia pulex feeding on Scenedesmus acutus of varying quality. Bull. mar. Sci. 53: 228-239.

    Google Scholar 

  • Stoecker, D. K. & J. M. Capuzzo, 1990. Predation on protozoa: its importance to zooplankton. J. Plankton Res. 12: 891-908.

    Google Scholar 

  • Stoecker, D. K. & G. T. Evans, 1985. Effects of protozoan herbivory and carnivory in a microplankton food web. Mar. Ecol. Prog. Ser. 25: 159-167.

    Google Scholar 

  • Stoecker, D. K., T. L. Cucci, E. M. Hulburt & C. M. Yentsch, 1986. Selective feeding by Balanion sp. (Ciliata: Balanionidae) on phytoplankton that best support its growth. J. exp. mar. Biol. Ecol. 95: 113-130.

    Google Scholar 

  • Stoecker, D. K., S. M. Gallager, C. J. Langdon & L. H. Davis, 1995. Particle capture by Favella sp. (Ciliata, Tintinnina). J. Plankton Res. 17: 1105-1124.

    Google Scholar 

  • Strom, S. L., 2001. Light-aided digestion, grazing and growth in herbivorous protists. Aquat. Microb. Ecol. 23: 253-261.

    Google Scholar 

  • Strom, S. L. & E. J. Buskey, 1993. Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda. Limnol. Oceanogr. 38: 965-977.

    Google Scholar 

  • Strom, S. L. & T. A. Morello, 1998. Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J. Plankton Res. 20: 571-584.

    Google Scholar 

  • Strom, S. L. & N. A. Welschmeyer, 1991. Pigment-specific rates of phytoplankton growth and microzooplankton grazing in the open subarctic Pacific Ocean. Limnol. Oceanogr. 36: 50-63.

    Google Scholar 

  • Strom, S. L., C. B. Miller & B. F. Frost, 2000. What sets the lower limits to phytoplankton biomass in high nitrate, low chlorophyll ocean regions? Mar. Ecol. Prog. Ser. 193: 19-31.

    Google Scholar 

  • Strom, S. L., G. V. Wolfe & A. Slajer, 2001. Phytoplankton DMSP release: a possible chemical defense against protist grazers? Abstract, American Society of Limnology and Oceanography, Albuquerque.

    Google Scholar 

  • Strom, S. L., G. V. Wolfe, J. Holmes, H. A. Stecher, S. Lambert & E. Moreno, submitted-a. Chemical defense in the microplankton I: feeding and growth of heterotrophic protists on the DMS-producing phytoplankter Emiliania huxleyi. Limnol. Oceanogr.

  • Strom, S. L., G. V. Wolfe, S. Lambert & J. Clough, submittedb. Chemical defense in the microplankton II: DMSP inhibits feeding in four heterotrophic protists. Limnol. Oceanogr.

  • Taniguchi, A. & Y. Takeda, 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.

    Google Scholar 

  • Tarran, G. A., 1991. Aspects of the feeding behaviour of the marine dinoflagellate Oxyrrhis marina Dujardin. Ph.D. thesis, Southampton Univ.

  • Taylor, F. J. R., 1987. Dinoflagellate morphology. In Taylor, F. J. R. (ed.), The Biology of Dinoflagellates. Blackwell Scientific, Oxford: 24-91.

    Google Scholar 

  • Tollrian, R. & C. D. Harvell (eds), 1999. The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton: 383 pp.

    Google Scholar 

  • Tranvik, L. J., E. B. Sherr & B. F. Sherr, 1993. Uptake and utilization of ‘colloidal DOM’ by heterotrophic flagellates in seawater. Mar. Ecol. Prog. Ser. 92: 301-309.

    Google Scholar 

  • Turner, J. T. & P. A. Tester, 1997. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol. Oceanogr. 42: 1203-1214.

    Google Scholar 

  • Van Donk, E., M. Lurling & W. Lampert, 1999. Consumer-induced changes in phytoplankton: inducibility, costs, benefits, and the impact on grazers. In Tollrian, R. & C. D. Harvell (eds), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton: 89-103.

    Google Scholar 

  • Venrick, E. L., J. A. McGowan, D. R. Cayan & T. L. Hayward, 1987. Climate and chlorophyll a: long-term trends in the central North Pacific ocean. Science 238: 70-72.

    Google Scholar 

  • Verity, P. G., 1986. Growth rates of natural tintinnid populations in Narragansett Bay. Mar. Ecol. Prog. Ser. 29: 117-126.

    Google Scholar 

  • Verity, P. G., 1991. Feeding in planktonic protozoans: evidence for non-random acquisition of prey. J. Protozool. 38: 69-76.

    Google Scholar 

  • Verity, P. G. & V. Smetacek, 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar. Ecol. Prog. Ser. 130: 277-293.

    Google Scholar 

  • Verity, P. G. & T. A. Villareal, 1986. The relative food value of diatoms, dinoflagellates, flagellates, and cyanobacteria for tintinnid ciliates. Arch. Protistenkd. 131: 71-84.

    Google Scholar 

  • Verity, P. G., D. K. Stoecker, M. E. Sieracki & J. R. Nelson, 1993. Grazing, growth and mortality of microzooplankton during the 1989 North Atlantic spring bloom at 47∘ N, 18∘ W. Deep-Sea Res. 40: 1793-1814.

    Google Scholar 

  • Verity, P. G., D. K. Stoecker, M. E. Sieracki & J. R. Nelson, 1996. Microzooplankton grazing of primary production at 140∘ W in the equatorial Pacific. Deep-Sea Res. II 43: 1227-1256.

    Google Scholar 

  • Walsh, J. J., 1976. Herbivory as a factor in patterns of nutrient utilization in the sea. Limnol. Oceanogr. 21: 1-13.

    Google Scholar 

  • Washburn, J. O., M. E. Gross, D. R. Mercer & J. R. Anderson, 1988. Predator-induced trophic shift of a free-living ciliate: parasitism of mosquito larvae by their prey. Science 240: 1193-1195.

    Google Scholar 

  • Weisse, T. & U. Scheffel-Möser, 1991. Uncoupling the microbial loop: growth and grazing loss rates of bacteria and heterotrophic nanoflagellates in the North Atlantic. Mar. Ecol. Prog. Ser. 71: 195-205.

    Google Scholar 

  • Wetherbee, R. & R. A. Andersen, 1992. Flagella of a chrysophycean alga play an active role in prey capture and selection. Protoplasma 166: 1-7.

    Google Scholar 

  • Wicklow, B. J., 1997. Signal-induced defensive phenotypic changes in ciliated protists: morphological and ecological implications for predator and prey. J. Euk. Microbiol. 44: 176-188.

    Google Scholar 

  • Wikner, J. & Å. Hagström, 1988. Evidence for a tightly coupled nanoplanktonic predator—prey link regulating the bacterivores in the marine environment. Mar. Ecol. Prog. Ser. 50: 137-145.

    Google Scholar 

  • Wolfe, G. V., 2000. The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impactsq. Biol. Bull. 198: 225-244.

    Google Scholar 

  • Wolfe, G. V. & M. Steinke, 1996. Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnol. Oceanogr. 41: 1151-1160.

    Google Scholar 

  • Wolfe, G. V., S. L. Strom, J. L. Holmes, T. Radzio & M. B. Olson, In press. In vivo DMSP cleavage by marine phytoplankton in response to physical, chemical, or dark stress. J. Phycol.

  • Zirbel, M. J. & S. L. Strom, 2001. Light-enhanced digestion by microzooplankton. Abstract, American Society of Limnology and Oceanography, Albuquerque.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Shannon Point Marine Center, Western Washington University, 1900 Shannon Point Rd., Anacortes, WA, 98221, U.S.A.

    Suzanne Strom

Authors
  1. Suzanne Strom
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Strom, S. Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea. Hydrobiologia 480, 41–54 (2002). https://doi.org/10.1023/A:1021224832646

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1021224832646

search

Navigation