Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T23:35:24.770Z Has data issue: false hasContentIssue false

Preliminary investigation on the phytoplankton contribution to the mussel diet on the basis of fatty acids analysis

Published online by Cambridge University Press:  25 July 2008

F. Biandolino*
Affiliation:
Institute for Coastal Marine Environment, Section of Taranto, CNR, Via Roma 3, 74100 Taranto, Italy
E. Prato
Affiliation:
Institute for Coastal Marine Environment, Section of Taranto, CNR, Via Roma 3, 74100 Taranto, Italy
C. Caroppo
Affiliation:
Institute for Coastal Marine Environment, Section of Taranto, CNR, Via Roma 3, 74100 Taranto, Italy
*
Correspondence should be addressed to: F. BiandolinoInstitute for Coastal Marine EnvironmentSection of Taranto CNR, Via Roma 3, 74100 TarantoItaly email: francesca.biandolino@iamc.cnr.it

Abstract

The composition of fatty acids was studied in the mussels collected in the Mar Grande of Taranto (northern Ionian Sea) during the four seasons. Micro-, nano- and picophytoplankton abundance, biomass and composition have been also evaluated. Fatty acids compositions were investigated for lipid biomarkers to establish the contribution of phytoplankton to the mussel diet. Saturated (SAFA) and monounsaturated fatty acids (MUFA) were the most abundant components, followed by polyunsaturated fatty acids (PUFA). The seasonal variations in the SAFAs, MUFAs and PUFAs were not significantly different during the whole study period (ANOVA, P < 0.05). The most abundant identified FAs were 16:0 (27.51–33.80% of total FAs), 14:1 (3.35–9.91% of total FAs), 18:1n9 (2.92–8.87%), 16:1 n7 (4.53– 7.61%) and 24:1n9 (0.43–8.84%). The most important PUFAs were 22:2 (2.35–3.48% of total FAs) and also 18:2n-6 (1.66–2.61%). PUFAs were characterized by low percentages of n3 and n6 FAs. Analysis of specific FA markers for diatoms (16:1n7, 20:5n3), phytoflagellates and dinoflagellates (16:0, 18:4n3) showed a negligible contribution of phytoplankton to the mussel diet.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Acosta Pomar, M.L. and Giuffrè, G. (1996) Pico-, nano- and microplankton communities in hydrothermal marine coastal environments of the Eolian Islands (Panarea and Vulcano) in the Mediterranean Sea. Journal of Plankton Research 18, 715730.Google Scholar
Albentosa, M., Pérez-Camacho, A., Labarta, U. and Fernández-Reiriz, M.J. (1996) Evaluation of live microalgal diets for the seed culture of Ruditapes decussatus using physiological and biochemical parameters. Aquaculture 148, 1123.CrossRefGoogle Scholar
Allinger, N.L., Cava, M.P., De Jough, D.C., Johnson, C.R., Lebel, N.A. and Stevens, C.L. (1986) Chimica organica. Bologna: Zanichelli.Google Scholar
Auel, H., Harjes, M., da Rocha, R., Stübing, D. and Hagen, W. (2002) Lipid biomarkers indicate different ecological niches and trophic relationship of the Arctic hyperiid amphipods Themisto abissorum and T. libellula. Polar Biology 25, 374383.CrossRefGoogle Scholar
Bayne, B. (1993) Feeding physiology of bivalves: time-dependence and compensation for changes in food availability. In Dame, R.F. (ed.) Bivalve filter feeders in estuarine and coastal ecosystem processes. NATO ASI Series G: Ecological Sciences, Volume 33. Heidelberg: Springer-Verlag, pp. 124.Google Scholar
Bell, M.V. and Sargent, J.R. (1985) Fatty acid analysis of phosphoglycerides from tissues of the clam Chlamys islandica (Müller) and the starfish Ctenodiscus crispatus (Retzius) from Balsfjorden, northern Norway. Journal of the Marine Biological Association of the United Kingdom 58, 825841.Google Scholar
Belmonte, G., Fanelli, G., Gravili, C. and Rubino, F. (2001) Composition, distribution and seasonality of zooplankton in Taranto seas (Ionian Sea, Italy). Biologia Marina Mediterranea 8, 352362.Google Scholar
Beninger, P.G. and Decottignies, P. (2005) What makes diatoms attractive for suspensivores? The organic casing and associated organic molecules of Coscinodiscus perforatus are quality cues for the bivalve Pecten maximus? Journal of Plankton Research 27, 1117.CrossRefGoogle Scholar
Besnard, J.Y. 1988. Etude des constituents lipidiques dans la gonade femelle et les larves de Pecten maximus L. (Mollusque Lamellibranche). Thése de Doctorat, Université de Caen, France, 154 pp.Google Scholar
Bradshaw, S.A., O'Hara, S.C.M., Corner, E.D.S. and Eglinton, G. (1991) Effects on dietary lipids of marine bivalve Scrobicularia plana feeding in different modes. Journal of the Marine Biological Association of the United Kingdom 71, 635653.CrossRefGoogle Scholar
Bricelj, V. and Shumway, S. (1991) Physiology. Energy acquisition and utilization. In Shumway, S. (ed.) Scallops: biology and aquaculture. Amsterdam: Elsevier Science Publishers BV, pp. 305345.Google Scholar
Brown, M.R., Jeffrey, S.W., Volkman, J.K. and Dunstan, G.A. (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151, 315331.CrossRefGoogle Scholar
Caers, M., Coutteau, P. and Sorgeloos, P. (2000) Impact of starvation and of feeding algal and artificial diets on the lipid content and composition of juvenile oysters (Crassostrea gigas) and clams (Tapes philippinarum). Marine Biology 136, 891899.CrossRefGoogle Scholar
Caron, D.A., Dam, H.G., Kremer, P., Lessard, E.J., Madin, L.P., Malone, T.C., Napp, J.M., Peele, E.R., Roman, M.R. and Youngbluth, M.J. (1995) The contribution of microorganisms to particulate carbon and nitrogen in surface waters of the Sargasso Sea near Bermuda. Deep-Sea Research 42, 943972.CrossRefGoogle Scholar
Caroppo, C. (2000) The contribution of picophytoplankton to community structure in a Mediterranean brackish environment. Journal of Plankton Research 22, 381397.CrossRefGoogle Scholar
Caroppo, C., Fiocca, A., Sammarco, P. and Magazzù, G. (1999) Seasonal variations of nutrients and phytoplankton in the coastal SW Adriatic Sea (1995–1997). Botanica Marina 42, 389400.CrossRefGoogle Scholar
Caroppo, C., Stabili, L., Aresta, M., Corinaldesi, C. and Danovaro, R. (2006a) Impact of heavy metals and PCBs on marine picoplankton. Environmental Toxicology 21, 541551.CrossRefGoogle ScholarPubMed
Caroppo, C., Turicchia, S. and Margheri, M.C. (2006b) Phytoplankton assemblages in coastal waters of the northern Ionian Sea (eastern Mediterranean), with special reference to cyanobacteria. Journal of the Marine Biological Association of the United Kingdom 86, 927937.CrossRefGoogle Scholar
Claustre, H., Marty, J.C., Cassiani, L. and Dagaud, J. (1989) Fatty acids dynamics in phytoplankton and microzooplankton communities during a spring bloom in the coastal Ligurian Sea: ecological implications. Marine Microbial Food Webs 3, 5166.Google Scholar
Cloern, J.E. (1982) Does the benthos control phytoplankton biomass in south San Francisco Bay? Marine Ecology Progress Series 9, 191202.CrossRefGoogle Scholar
Conway, N. and McDowell Capuzzo, J. (1991) Incorporation and utilization of bacteria lipids in the Solemya velum symbiosis. Marine Biology 108, 277292.CrossRefGoogle Scholar
Cripps, G.C., Watkins, J.L., Hill, H.J. and Atkinson, A. (1999) Fatty acid content of Antarctic krill, Euphasia superba, at South Georgia related to regional populations and variations in diet. Marine Ecology Progress Series 181, 177188.CrossRefGoogle Scholar
Dame, R.F. (1996) Ecology of marine bivalves. Boca Raton, FL: CRC Press, pp. 254.CrossRefGoogle Scholar
Davenport, J., Smith, R.J.J.W. and Packer, M. (2000) Mussels Mytilus edulis: significant consumers and destroyers of mesozooplankton. Marine Ecology Progress Series 198, 131137.CrossRefGoogle Scholar
Dunstan, G.A., Volkman, J.K., Barrett, S.M., Leroi, J.M. and Jeffrey, S.W. (1994) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochemistry 35, 155161.CrossRefGoogle Scholar
Dupuy, C., Vaquer, A., Lam-Hoai, T., Rougier, C., Mazouni, N., Lautier, J., Collos, Y. and Le Gall, S. (2000) Feeding rate of the oyster Crassostrea gigas in a natural planktonic community of the Mediterranean Thau Lagoon. Marine Ecology Progress Series 205, 171184.CrossRefGoogle Scholar
Fahl, K. and Kattner, G. (1993) Lipid content and fatty acid composition of algal communities in sea-ice and water from the Weddell Sea (Antarctica). Polar Biology 13, 405409.CrossRefGoogle Scholar
Falk-Petersen, S., Dahl, T.M., Scott, C.L., Sargent, J.R., Gulliksen, B., Kwasniewski, S., Hop, H. and Millar, R.M. (2002) Lipid biomarkers and trophic linkages between ctenophores and copepods in Svalbard waters. Marine Ecology Progress Series 227, 187194.CrossRefGoogle Scholar
FAO (1989) Report of the workshop and study tour on mollusc sanitation and marketing. (http://www.fao.org/docrep/field/003/AB710E/AB710E00.HTM)Google Scholar
Fernanadez-Reiriz, M.J., Labarta, U. and Babarro, J.M.F. (1996) Comparative allometries in growth and chemical composition of mussel (Mytilus galloprovincialis Lmk) cultured in two zones in the Ria sada (Galicia, NW Spain). Journal of Shellfish Research 15, 349353.Google Scholar
Folch, J., Lees, M. and Sloane-Stanley, G.H. (1957) A simple method for the isolation and purification of total lipids from animal tissue. Journal of Biological Chemistry 226, 497509.CrossRefGoogle Scholar
Fonda Umani, S., Franco, P., Ghirardelli, E. and Malej, A. (1992) Outline of oceanography and the plankton of the Adriatic Sea. In Colombo, G., Ferrari, I., Ceccherelli, V.U. and Rossi, R. (eds) Marine eutrophication and population dynamics. Freensborg: Olsen and Olsen, pp. 347365.Google Scholar
Freites, L., Fernández-Reiriz, M.J. and Labarta, U. (2002) Fatty acid profiles of Mytilus galloprovincialis (Lmk) mussel of subtidal and rocky shore origin. Comparative Biochemistry and Physiology 132, 453461.CrossRefGoogle ScholarPubMed
Gillan, F.T. and Johns, R.B. (1986) Chemical markers for marine bacteria: fatty acids and pigments. In Johns, R.B. (ed.) Biological markers in the sedimentary environment. Amsterdam: Elsevier Science Publisher BV, pp. 291309.Google Scholar
Graeve, M., Hagen, W. and Kattner, G. (1994) Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods. Deep-Sea Research 41, 915924.CrossRefGoogle Scholar
Hunter, B.L. and Laws, E.A. (1981) ATP and chlorophyll a as estimators of phytoplankton carbon biomass. Limnology and Oceanography 26, 944956.CrossRefGoogle Scholar
Joseph, J.D. (1982) Lipid composition of marine and estuarine invertebrates. Part II: Mollusca. Progress in Lipid Research 22, 109153.CrossRefGoogle Scholar
Kharlamenko, V.I., Zhukova, N.V., Khotimchenko, S.V.Svetaschev, V.I. and Kamenev, G.M. (1995) Fatty acids as markers of food sources in shallow-water hydrothermal ecosystems (Kraternaya Bight, Yankich Island, Kurile Islands). Marine Ecology Progress Series 120, 231241.CrossRefGoogle Scholar
Kharlamenko, V.I., Kiyashko, S.I., Imbs, A.B. and Vyshkvartzev, D.I. (2001) Identification of food source of invertebrates from the sea grass Zostera marina community using carbon and sulphur stable isotope ratio and fatty acid analyses. Marine Ecology Progress Series 220, 103117.CrossRefGoogle Scholar
Klingensmith, J.S. (1982) Distribution of methylene and non methylene-interrupted dienoic fatty acids in polar lipids and triacylglycerols of selected tissue of the hard-shell clam (Mercenaria mercenaria). Lipids 17, 976981.CrossRefGoogle Scholar
Knox, G.A. (1986) Estuarine ecosystems: a systems approach. Volume I. Boca Raton, FL: CRC Press, pp. 198.Google Scholar
Kreeger, D.A. and Newell, R.I.E. (2001) Seasonal utilization of different seston carbon sources by the ribbed mussel, Geukensia demissa (Dillwyn) in a mid-Atlantic salt marsh. Journal of Experimental Marine Biology and Ecology 260, 7191.CrossRefGoogle Scholar
Lee, S.J., Yoon, B.D. and Oh, H.M. (1998) Rapid method for the determination of lipid from the green alga Botryococcus braunii. Biotechnology Techniques 12, 553556.CrossRefGoogle Scholar
Le Gall, S, Hassen, M.B. and Le Gall, P. (1997) Ingestion of a bacterivorous ciliate by the oyster Crassostrea gigas: protozoa as a trophic link between picoplankton and benthic suspension feeders. Marine Ecology Progress Series 152, 301306.CrossRefGoogle Scholar
Lehane, C. and Davenport, J. (2002) Ingestion of mesozooplankton by three species of bivalve: Mytilus edulis, Cerastoderma edule and Aequipecten opercularis. Journal of the Marine Biological Association of the United Kingdom 82, 615619.CrossRefGoogle Scholar
Mansour, M.P., Volkman, J.K., Jackson, A.E. and Blackburn, S.I. (1999) The fatty acid and sterol composition of five marine dinoflagellates. Journal of Phycology 35, 710720.CrossRefGoogle Scholar
Matarrese, A., Tursi, A., Costantino, G. and Pollicoro, R. (1993) The reproductive cycle of Mytilus galloprovincialis Lamarck in the Mar Piccolo and in the Mar Grande of Taranto (Ionian sea). Oebalia 19, 111.Google Scholar
Maugeri, T.L., Acosta Pomar, L. and Bruni, V. (1990) Picoplancton. Nova Thalassia 11, 199205.Google Scholar
Mac Donald, B. and Ward, J. (1994) Variation in food quality and particle selectivity in the sea scallop Placopecten magellanicus (Mollusca: Bivalvia). Marine Ecology Progress Series 108, 251264.CrossRefGoogle Scholar
Molina, E., Martínez, M.E., Sánchez, S., García, F. and Contreras, A. (1991) Growth and biochemical composition with emphasis on the fatty acids of Tetraselmis sp. Applied Microbiology and Biotechnology 36, 2125.CrossRefGoogle Scholar
Nelson, M.M., Mooney, B.D., Nichols, P.D. and Phleger, C.F. (2001) Lipids of Antarctic amphipods: food chain interactions and the occurrence of novel biomarkers. Marine Chemistry 73, 5364.CrossRefGoogle Scholar
Nichols, D.S., Nichols, P.D. and Sullivan, C.W. (1993) Fatty acid, strol and hydrocarbon composition of Antarctic sea ice diatom communities during the spring bloom in McMurdo Sound. Antarctic Science 5, 271278.CrossRefGoogle Scholar
Officer, C.B., Smayda, T.J. and Mann, R. (1982) Benthic filter feeding: a natural eutrophication control. Marine Ecology Progress Series, 9 (2), 203210.CrossRefGoogle Scholar
Ogilvie, S.C., Ross, A.H., James, M.R. and Schiel, D.R. (2003) In situ enclosure experiments on the influence of cultivated mussels (Perna caniliculus) on phytoplankton at times of high and low ambient nitrogen. Journal of Experimental Marine Biology and Ecology 295, 2339.CrossRefGoogle Scholar
Parsons, T.R., Maita, Y. and Lalli, C.M. (1984) A manual of chemical and biological methods for seawater analysis. Oxford: Pergamon Press, pp. 173.Google Scholar
Pastore, M., Panetta, P., Andreoli, C. and Dell'Angelo, B. (1976) Accrescimento di Mytilus galloprovincialis (Lam.) nei mari di Taranto. Oebalia 2, 2061.Google Scholar
Perry, G.J., Volkman, J.K. and Johns, Jr R.B. (1979) Fatty acids of bacterial origin in contemporary marine sediments. Geochimica et Cosmochimica Acta 43, 17151725.CrossRefGoogle Scholar
Pond, D.P., Bell, M.V., Dixon, D.R., Fallick, A.E., Segonzac, M. and Sargent, J. (1998) Stable-carbon-isotope composition of fatty acids in hydrothermal vent mussels containing methano-trophic and thiotrophic bacterial endosymbionts. Applied and Environmental Microbiology 64, 370375.CrossRefGoogle ScholarPubMed
Prins, T.C., Smaal, A.C. and Pouwer, A.J. (1991) Selective ingestion of phytoplankton by the bivalves Mytilus edulis L. and Cerastoderma edule (L.). Hydrobiological Bulletin 25, 93100.CrossRefGoogle Scholar
Renaud, S.M., Thinh, L.V. 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, 147159.CrossRefGoogle Scholar
Rodhouse, P.G., Roden, C.M., Burnell, G.M., Hensey, M.P., McMahon, T., Ottway, B. and Ryan, T.H. (1984) Food resource, gametogenesis and growth of Mytilus edulis on the shore and in suspended culture: Killary Harbour, Ireland. Journal of the Marine Biological Association of the United Kingdom 64, 513529.CrossRefGoogle Scholar
Roditi, H.A., Fisher, N.S. and Sando-Wilhelmy, S.A. (2000) Uptake of dissolved organic carbon and trace elements by zebra mussels. Nature 407, 7880.CrossRefGoogle ScholarPubMed
Safi, K.A. and Gibbs, M.M. (2003) The importance of different size classes of phytoplankton in Beatrix Bay, Pelorus Sound and the potential implications for the aquaculture of the mussel Perna canaliculus. New Zealand Journal of Marine and Freshwater Research 37, 267272.CrossRefGoogle Scholar
Sargent, J.R. (1976) The structure, metabolism and function of lipids in marine organisms. In Malins, D.C. and Sargent, J.R. (eds.) Biochemical and biophysical perspectives in marine biology. London: Academic Press vol. III, pp. 149212.Google Scholar
Sargent, J.R. and Whittle, K.J. (1981) Lipids and hydrocarbons in the marine food web. In Longhurst, A. (ed.) Analysis of marine ecosystems. Academic Press: London, pp. 491533.Google Scholar
Sargent, J.R., Bell, M.V., Henderson, R.J. and Tocher, D.R. (1990) Polyunsaturated fatty acids in the marine and terrestrial food webs. In Animal Nutrition and transport processes. Part I. Nutrition in wild and domestic animals 5, 1123.Google Scholar
Shumway, S., Cucci, T., Newell, R. and Yentsch, C. (1985) Particle selection, ingestion, and absorption in filter-feeding bivalves. Journal of Experimental Marine Biology and Ecology 91, 7792.CrossRefGoogle Scholar
Shumway, S.E., Selvin, R. and Schick, D.F. (1987) Food resources related to habitat in the scallop Placopecten magellanicus (Gmelin, 1791): a qualitative study. Journal of Shellfish Research 6, 8995.Google Scholar
Sieracki, M.E., Viles, C.L. and Webb, K.L. (1989) Algorithm to estimate cell biovolume using image analyzed microscopy. Cytometry 10, 551557.CrossRefGoogle ScholarPubMed
Socal, G., Boldrin, A., Bianchi, F., Civitarese, G., De Lazzari, A., Rabitti, S., Totti, C. and Turchetto, M. (1999) Nutrient, particulate matter and phytoplankton variability in the photic layer of the Otranto strait. Journal of Marine Systems 20, 381398.CrossRefGoogle Scholar
Søndergaard, M., Jensen, L.M. and Ærtebjerg, G. (1991) Picoalgae in Danish coastal waters during summer stratification. Marine Ecology Progress Series 79, 139149.CrossRefGoogle Scholar
Urrutia, M.B., Iglesias, J.I.P., Navarro, E. and Prou, J. (1996) Feeding and absorption in Cerastoderma edule under environmental conditions in the bay of Marennes-Oleron (Western France). Journal of the Marine Biological Association of the United Kingdom 76, 431450.CrossRefGoogle Scholar
Utermöhl, H. (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilungen Internationale Vereins Theoretisch Angewiesen Limnologie 9, 138.Google Scholar
Vanucci, S., Acosta Pomar, M.L.C. and Maugeri, T.L. (1994) Seasonal pattern and phototrophic picoplankton in the eutrophic coastal waters of the Northern Adriatic Sea. Botanica Marina 37, 5766.CrossRefGoogle Scholar
Vilicic, D., Leder, N., Grzetic, Z. and Jasprica, N. (1995) Microphytoplankton in the Strait of Otranto (eastern Mediterranean). Marine Biology 123, 619630.CrossRefGoogle Scholar
Virtue, P., Nichols, P.D., Nicol, S., McMinn, A. and Sikes, E.L. (1993) The lipid composition of Euphasia superba Dana in relation to the nutritional value of Phaeocystis pouchetii (Hariot) Lagerheim. Antarctic Science 5, 169177.Google Scholar
Volkman, J.K., Jeffrey, S.W., Nichols, P.D., Rogers, G.I. and Garland, C.D. (1989) Fatty acid and lipid composition of 10 species of microalgae used in mariculture. Journal of Experimental Marine Biology and Ecology 128, 219240.CrossRefGoogle Scholar
Von Elert, E. and Wolffrom, T. (2001) Supplementation of cyanobacterial food with polyunsaturated fatty acids does not improve growth of Daphnia. Limnology and Oceanography 46, 15521558.CrossRefGoogle Scholar
Voogt, P.A. (1983) Lipids: their distribution and metabolism. In Hochachka, P.W. (ed.) The Mollusca. I. New York: Academic Press, pp. 329370.Google Scholar
Welschmeyer, N.A. and Lorenzen, C.J. (1984) Carbon-14 labelling of phytoplankton carbon and chlorophyll a carbon: determination of specific growth rates. Limnology and Oceanography 29, 135145.CrossRefGoogle Scholar
Whyte, J.N.C. (1988) Fatty acid profiles from direct methanolysis of lipids in tissue of cultured species. Acquaculture 75, 193203.CrossRefGoogle Scholar
Wong, W.H., Levinton, J.S., Twining, B.S. and Fisher, N.S. (2003a) Assimilation of micro- and mesozooplankton by zebra mussels: a demonstration of the food web link between zooplankton and benthic suspension feeders. Limnology and Oceanography 48, 308312.CrossRefGoogle Scholar
Wong, W.H., Levinton, J.S., Twining, B.S., Fisher, N.S., Kelaher, B.P. and Alt, A.K. (2003b) Carbon assimilation from rotifer Brachionus plicatilis by mussels, Mytilus edulis and Perna viridis: a potential food web link between zooplankton and benthic suspension feeders in the marine system. Marine Ecology Progress Series 253, 175182.CrossRefGoogle Scholar
Zeldis, J., Robinson, K., Ross, A. and Hayden, B. (2004) First observations of predation by New Zealand greenshell mussels (Perna canaliculus) on zooplankton. Journal of Experimental Marine Biology and Ecology 311, 287299.CrossRefGoogle Scholar
Zhukova, N.V. (1991) The pathway of the biosynthesis of non-methylene-interrupted dienoic fatty acids in molluscs. Comparative Biochemistry and Physiology 100B, 801804.Google Scholar