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Seasonal relative influence of food quantity, quality, and feeding behaviour on zooplankton growth regulation in coastal food webs

Published online by Cambridge University Press:  19 October 2009

C.A. Vargas ,
R.A. Martínez ,
R. Escribano  and
N.A. Lagos
C.A. Vargas*
Affiliation:
Aquatic System Unit, Environmental Sciences Center EULA Chile, Universidad de Concepción, PO Box 160-C, Concepción, Chile
R.A. Martínez
Affiliation:
Aquatic System Unit, Environmental Sciences Center EULA Chile, Universidad de Concepción, PO Box 160-C, Concepción, Chile
R. Escribano
Affiliation:
Department of Oceanography andCenter for Oceanographic Research in the Eastern South Pacific, Universidad de Concepción, P O Box 160-C, Concepción, Chile
N.A. Lagos
Affiliation:
Departamento de Ciencias Básicas andCentro de Investigación en Ciencias Ambientales (CIENCIA-UST), Universidad Santo Tomás, Ejercito 146, Santiago, Chile
*
Correspondence should be addressed to: C.A. Vargas, Aquatic System Unit, Environmental Sciences Center EULA Chile, Universidad de Concepción, PO Box 160-C, Concepción, Chile email: [email protected]
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Abstract

In aquatic food webs zooplankton constitutes an important link between primary producers and higher trophic levels. Copepods often dominate the zooplankton in coastal oceans and are the prey of the majority of planktivorous fish. Feeding behaviour, as well as the food quantity and quality are recognized factors that affect copepod growth, and therefore, the energy transfer efficiency throughout food webs. The natural occurrence and magnitude of these growth factors and their combined effects on marine copepods, as keystone grazers in the pelagic marine realm, are poorly understood. Here, we assessed how these different factors vary throughout the year, and then examine their relative influence upon copepods maximal growth rates. A multiple regression model, including all variables previously selected, and the inclusion of the sea temperature allowed us to estimate the pure influence of the studied factors, and the environmental effect on copepod growth rates. The results imply that ingestion of diatoms may induce a positive effect on specific growth rates of copepods, and the quality of this food item (high PUFA and HUFA availability) might explain such effect. Therefore, seasonal variability in diatom abundance, possibly driven by changes in the oceanographic regime, should be considered a critical factor controlling copepod growth in productive coastal ecosystems.

Keywords

food quantityfood qualityfatty acidsdiatomsdinoflagellateszooplankton growthfood websupwelling
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 90 , Special Issue 6: In Honour of Sir Frederick Stratten Russell, FRS , September 2010 , pp. 1189 - 1201
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Berge, J.P., Gouygou, J.P., Dubacq, J.P. and Durand, P. (1995) Reassessment of lipid composition of the diatom Skeletonema costatum. Phytochemistry 39, 1017–1021.Google Scholar
Bergreen, U., Hansen, B. and Kiørboe, T. (1988) Food size spectra, ingestion and growth of the copepod Acartia tonsa during development: implications for determination of copepod production. Marine Biology 99, 341–352.Google Scholar
Brett, M.T. and Müller-Navarra, D.C. (1997) The role of highly unsaturated fatty acids in aquatic food web processes. Freshwater Biology 38, 483–499.CrossRefGoogle Scholar
Cushing, D.H. (1989) A difference in structure between ecosystems in strongly stratified waters and in those that are weakly stratified. Journal of Plankton Research 11, 1–13.CrossRefGoogle Scholar
Edler, L. (1979) Recommendations for marine biological studies in the Baltic Sea. The Baltic Marine Biologist Publications 5, 1–38.Google Scholar
Elser, J.J. and Hassett, R.I. (1994) A stoichiometric analysis of zooplankton–phytoplankton interactions in marine and freshwater systems. Nature 370, 211–213.Google Scholar
Escribano, R. and McLaren, I.A. (1999) Production of Calanus chilensis from the upwelling area of Antofagasta, northern Chile. Marine Ecology Progress Series 177, 147–156.CrossRefGoogle Scholar
Fraser, A.J., Sargent, J.R., Gamble, J.C. and Seaton, D.D. (1989) Formation and transfer of fatty acids in an enclosed marine food chain comprising phytoplankton, zooplankton and herring (Clupea harengus) larvae. Marine Chemistry 27, 1–18.CrossRefGoogle Scholar
Freckleton, R.P. (2002) Chaotic mating systems. Trends in Ecology and Evolution 17, 493–495.Google Scholar
Frost, B.W. (1972) Effect of size and concentration of food particles on the feeding behaviour of the marine planktonic copepod Calanus pacificus. Limnology and Oceanography 17, 805–815.CrossRefGoogle Scholar
Guisande, C., Riveiro, I. and Maneiro, I. (2000) Comparisons among the amino acid composition of females, eggs and food to determine the relative importance of food quantity and food quality to copepod reproduction. Marine Ecology Progress Series 202, 135–142.Google Scholar
Haas, L.W. (1982) Improved epifluorescence microscopy for observing planktonic microorganisms. Annales de l'Institut Océanographique 58, 261–266.Google Scholar
Hansen, P.J., Bjørnsen, P.K. and Hansen, B.W. (1997) Zooplankton grazing and growth: scaling within the 2–2,000-µm body size range. Limnology and Oceanography 42, 687–704.Google Scholar
Hassett, P.R. (2004) Supplementation of a diatom diet with cholesterol can enhance copepod egg-production rates. Limnology and Oceanography 49, 488–494.Google Scholar
Hidalgo, P. and Escribano, R. (2007) Coupling of life cycles of the copepods Calanus chilensis and Centropages brachiatus to upwelling induced variability in the central-southern region of Chile. Progress in Oceanography 75, 501–517.CrossRefGoogle Scholar
Hirst, A.G. and Kiørboe, T. (2002) Mortality of marine planktonic copepods: global rates and patterns. Marine Ecology Progress Series 230, 195–209.CrossRefGoogle Scholar
Hirst, A.G., Peterson, W.T. and Rothery, R. (2005) Errors in juvenile copepod growth rate estimates are widespread: problems with the moult rate method. Marine Ecology Progress Series 296, 263–279.CrossRefGoogle Scholar
Huntley, M.E. and Lopez, M.D.G. (1992) Temperature-dependent production of marine copepods—a global synthesis. The American Naturalist 140, 201–242.CrossRefGoogle Scholar
Ianora, A., Miralto, A., Poulet, S.A., Carotenuto, Y., Buttino, I., Romano, G., Casotti, R., Pohnert, G., Wichard, T., Colucci D' Amato, L., Terrazzano, G. and Smetacek, V. (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429, 403–407.Google Scholar
Irigoien, X., Harris, R.P., Verheye, H.M., Joly, P., Runge, J., Starr, M., Pond, D., Campbell, R., Shreeve, R., Ward, P., Smith, A.N., Dam, H.G., Peterson, W., Tirelli, V., Koski, M., Smith, T., Harbour, D. and Davidson, R. (2002) Copepod hatching success in marine ecosystems with high diatom concentrations—the paradox of diatom–copepod interactions revisited. Nature 419, 387–389.CrossRefGoogle Scholar
Jónasdóttir, S.H. (1994) Effects of food quality on the reproductive success of Acartia tonsa and Acartia hudsonica: laboratory observations. Marine Biology 121, 67–81.CrossRefGoogle Scholar
Jónasdóttir, S.H., Fields, D. and Pantoja, S. (1995) Copepod egg production in Long Island Sound, USA, as a function of the chemical composition of seston. Marine Ecology Progress Series 119, 87–98.Google Scholar
Jónasdóttir, S.H., Gudfinnsson, H.G., Gislason, A. and Astthorsson, O.S. (2002) Diet composition and quality for Calanus finmarchicus egg production and hatching success off southwest Iceland. Marine Biology 140, 1195–1206.Google Scholar
Jones, R.H., Flynn, K.J. and Anderson, T.R. (2002) The effect of food quality on carbon and nitrogen growth efficiency in Acartia tonsa. Marine Ecology Progress Series 235, 147–156.Google Scholar
Kainz, M., Arts, M.T. and Mazumder, A. (2004) Essential fatty acid in the planktonic food web: their ecological role for higher trophic levels. Limnology and Oceanography 49, 1784–1793.CrossRefGoogle Scholar
Kattner, G., Cercken, G. and Eberlein, K. (1983) Development of lipid during a spring bloom in the northern North Sea. I. Particulate fatty acids. Marine Chemistry 14, 149–162.CrossRefGoogle Scholar
Kattner, G. and Fricke, H.S.G. (1986) Simple gas–liquid chromatographic method for the simultaneous determination of fatty acids and alcohols in wax esters of marine organisms. Journal of Chromatography 361, 263–268.CrossRefGoogle Scholar
Kimmerer, W.J. and McKinnon, A.D. (1989) Zooplanton in a marine bay. III. Evidence for influence of vertebrate predation on distribution of two common copepods. Marine Ecology Progress Series 53, 21–35.Google Scholar
Klein Breteler, W.C.M., Schogt, N., Baas, M., Schouten, S. and Kraay, G.W. (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Marine Biology 135, 191–198.CrossRefGoogle Scholar
Kleppel, G.S., Burkart, C.A. and Houchin, L. (1998) Nutrition and the regulation of egg production in the calanoid copepod Acartia tonsa. Limnology and Oceanography 43, 1000–1007.CrossRefGoogle Scholar
Kleppel, G.S. and Hazzard, S.E. (2000) Diet and egg production of the copepod Acartia tonsa in Florida Bay. II. Role of the nutritional environment. Marine Biology 137, 111–121.Google Scholar
Lagos, N.A., Castilla, J.C. and Broitman, B.R. (2008) Spatial environmental correlates of intertidal recruitment: a test using barnacles in northern Chile. Ecological Monographs 78, 245–261.Google Scholar
Lavaniegos, B.E. and López-Córtez, D. (1997) Fatty acid composition and community structure of plankton from the San Lorenzo Channel, Gulf of California. Estuarine, Coastal and Shelf Science 45, 845–854.CrossRefGoogle Scholar
Longhurst, A.R. (1985) The structure and evolution of plankton communities. Progress in Oceanography 15, 1–35.CrossRefGoogle Scholar
Lotka, A.J. (1925) Elements of physical biology. Baltimore, MD: Williams and Wilkins Company, 460 pp.Google Scholar
Marie, D., Partensky, F., Jacquet, S. and Vaulot, D. (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Applied and Environmental Microbiology 63, 186–93.Google Scholar
Marín, V., Huntley, M.E. and Frost, B. (1986) Measuring feeding rates of pelagic herbivores: analysis of experimental design and methods. Marine Biology 93, 49–58.Google Scholar
Mayzaud, P., Chanut, J.P. and Ackman, R.G. (1989) Seasonal changes of the biochemical composition of marine particulate matter with special reference to fatty acids and sterols. Marine Ecology Progress Series 56, 189–204.Google Scholar
Miller, C.B., Johnson, J.K. and Heinle, D.R. (1977) Growth rules in the marine copepod genus Acartia. Limnology and Oceanography 22, 326–335.CrossRefGoogle Scholar
Miralto, A., Barone, G., Romano, G., Poulet, S.A., Ianora, A., Russo, L., Buttino, I., Mazzarella, G., Laabir, M., Cabrini, M. and Giacobbe, M.G. (1999) The insidious effect of diatoms on copepod reproduction. Nature 402, 173–176.Google Scholar
Moreno, V.J., Moreno, J.E.A. and Brenner, R.R. (1979) Fatty acid metabolism of the calanoid copepod Paracalanus parvus. 2. Palmitate, stearate, oleate and acetate. Lipids 14, 318–322.Google Scholar
Ohman, M.D. and Snyder, R.A. (1991) Growth kinetics of the omnivorous oligotrich ciliate Strombidium sp. Limnology and Oceanography 36, 922–935.CrossRefGoogle Scholar
Peterson, W.T., Tiselius, P. and Kiørboe, T. (1991) Copepod egg production, moulting and growth rates, and secondary production, in the Skagerrak in August 1988. Journal of Plankton Research 13, 131–154.Google Scholar
Pond, D., Harris, R., Head, R. and Harbour, D. (1996) Environmental and nutritional factors determining seasonal variability in the fecundity and egg viability of Calanus helgolandicus in coastal waters off Plymouth, UK. Marine Ecology Progress Series 143, 45–63.Google Scholar
Poulet, S.A., Wichard, T., Ledoux, J.B., Lebreton, B., Marchetti, J., Dancie, C., Bonnet, D., Cueff, A., Morin, P. and Pohnert, G. (2006) The influence of diatoms on copepod reproduction. I. New field and laboratory observations related to Calanus helgolandicus egg production. Marine Ecology Progress Series 308, 129–142.CrossRefGoogle Scholar
Renaud, S.M., Van Thinh, L. and Parry, D.L. (1999) The gross chemical composition and fatty acid composition of 18 species of tropical Australian microalgae for possible use in mariculture. Aquaculture 170, 147–159.Google Scholar
Richardson, A.J. and Verheye, H.M. (1998) The relative importance of food and temperature to copepod egg production and somatic growth in the southern Benguela upwelling system. Journal of Plankton Research 20, 2379–2399.Google Scholar
SAS Institute (1996) Statistical analysis system: user's guide. Cary, NC: SAS Institute, 956 pp.Google Scholar
Sieburth, J.McN., Smetacek, V. and Lentz, J. (1978) Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology and Oceanography 23, 1256–1263.CrossRefGoogle Scholar
Stoecker, D.K., Gifford, D.J. and Putt, M. (1994) Preservation of marine planktonic ciliates: losses and cell shrinkage during fixation. Marine Ecology Progress Series 110, 293–299.Google Scholar
Strickland, J.D. and Parsons, T.R. (1972) A practical handbook of seawater analysis. Bulletin. Fisheries Research Board of Canada, 310 pp.Google Scholar
Sul, D., Kaneshiro, E.S., Jayasimhulu, K. and Erwin, J.A. (2000) Neutral lipids, their fatty acids, and the sterols of the marine ciliated protozoon, Parauronema acutum. Journal of Eukaryotic Microbiology 47, 373–378.CrossRefGoogle ScholarPubMed
Tabachnick, B.G. and Fidel, L.S. (1989) Using multivariate statistics. New York: Harper and Row, 746 pp.Google Scholar
Tang, K.W.H., Jakobsen, H. and Visser, A.W. (2001) Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: feeding, growth, and trophic interactions among grazers. Limnology and Oceanography 46, 1860–1870.Google Scholar
Tiselius, P. (1992) Behavior of Acartia tonsa in patchy food environments. Limnology and Oceanography 37, 1640–1651.Google Scholar
Touratier, F., Legendre, L. and Vezina, A. (1999) Model of copepod growth influenced by the food carbon:nitrogen ratio and concentration, under the hypothesis of strict homeostasis. Journal of Plankton Research 21, 1111–1132.Google Scholar
Turner, J.T. (2002) Zooplankton fecal pellets, marine snow and sinking phytoplankton blooms. Aquatic Microbial Ecology 27, 57–102.CrossRefGoogle Scholar
Utermöhl, H. (1958) Zur Vervollkommung der quantitativen Phytoplankton-Methodik. Mitteilungen. Internationale Vereiningung für Theoretische und Angewandte Limnologie 9, 1–39.Google Scholar
Vargas, C.A. and González, H.E. (2004) Plankton community structure and carbon cycling in a coastal upwelling system. I. Bacteria, microprotozoans and phytoplankton in the diet of copepods and appendicularians. Aquatic Microbial Ecology 34, 151–164.Google Scholar
Vargas, C.A., Escribano, R. and Poulet, S.A. (2006) Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses. Ecology 87, 2992–2999.CrossRefGoogle ScholarPubMed
Vargas, C.A., Martínez, R., Cuevas, L., Pavez, M., Cartes, C., González, H., Escribano, R. and Daneri, G. (2007) The relative importance of microbial and classical food webs in a highly productive coastal upwelling area. Limnology and Oceanography 52, 1495–1510.Google Scholar
Vargas, C.A., Martínez, R.A., González, H.E. and Silva, N. (2008) Contrasting trophic interactions of microbial and copepod communities in a fjord ecosystem, Chilean Patagonia. Aquatic Microbial Ecology 53, 227–242.Google Scholar
Verity, P.G. and Paffenhöfer, G.A. (1996) On assessment of prey ingestion by copepods. Journal of Plankton Research 18, 1767–1779.Google Scholar
Ying, L., Kang-sen, M. and Shi-chun, S. (2000) Total lipid and fatty acid composition of eight strains of marine diatoms. Chinese Journal of Oceanology and Limnology 18, 345–349.Google Scholar