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Trophic resources of the bivalve, Venusverrucosa, in the Chausey archipelago (Normandy, France) determined by stableisotopes and fatty acids

Published online by Cambridge University Press:  08 July 2013

Véronique Perez
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1 Canada
Frédéric Olivier
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1 Canada Muséum National d’Histoire Naturelle, DMPA, UMR 7208 BOREA CNRS-P6-MNHN-IRD, 61 rue Buffon, 75231 Paris, France
Réjean Tremblay*
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1 Canada
Urs Neumeier
Affiliation:
Institut des sciences de la mer, Université du Québec à Rimouski, 310 allée des Ursulines, Rimouski, Québec, G5L 3A1 Canada
Julien Thébault
Affiliation:
Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, LEMAR, UMR 6539, UBO-IRD-CNRS, Technopôle Brest-Iroise, rue Dumont d’Urville, 29280 Plouzané, France
Laurent Chauvaud
Affiliation:
Institut Universitaire Européen de la Mer, Université de Bretagne Occidentale, LEMAR, UMR 6539, UBO-IRD-CNRS, Technopôle Brest-Iroise, rue Dumont d’Urville, 29280 Plouzané, France
Tarik Meziane
Affiliation:
Muséum National d’Histoire Naturelle, DMPA, UMR 7208 BOREA CNRS-P6-MNHN-IRD, 61 rue Buffon, 75231 Paris, France
*
a Corresponding author:[email protected]
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Abstract

In the Chausey archipelago, growth of the burrowing bivalve Venus verrucosa(Mollusca: Veneridae) has been shown to be highly variable between closelylocated sites (<1 km). To explain this small-scale spatial variability, we tested thetrophic hypothesis using both fatty acid markers, and carbon and nitrogen stable isotopes(δ13C and δ15N). Environmentalparameters, including substrate, were also analysed to discriminate their effects onpotential trophic differences. Results of isotopic fractionation and lipid profiles ofwater column and digestive gland samples both showed a large contribution of phytoplanktonto the diet of V. verrucosa. More surprisingly, the same results suggestthat Phaeophyceae and Rhodophyceae macroalgae could contribute to the nutrition ofV. verrucosa as dissolved exudates. Whereas site differences were notobserved between the food sources of V. verrucosa, we showed that growthperformance index was correlated to wave height. Thus, we hypothesized that the high localgrowth variability could be controlled by the hydrosedimentary dynamics. In addition,although no significant growth differences were found between intertidal and subtidalpopulations, better condition index and more total lipids were found in the digestivegland of intertidal V. verrucosa, suggesting potential compensatorygrowth mechanisms.

Type
Research Article
Copyright
© EDP Sciences, IFREMER, IRD 2013

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References

Alber, M., Valiela, I., 1996, Utilization of microbial organic aggregates by bay scallops, Argopecten irradians (Lamarck). J. Exp. Mar. Biol. Ecol. 195, 7189. CrossRefGoogle Scholar
Almada-Villela, P.C., Davenport, J., Gruffydd, L.D., 1982, The effects of temperature on the shell growth of young Mytilus edulis L. J. Exp. Mar. Biol. Ecol. 59, 275288. CrossRefGoogle Scholar
Amouroux, J.M., 1984, Preliminary study on the consumption of dissolved organic matter (exudates) of bacteria and phytoplankton by the marine bivalve Venus verrucosa. Mar. Biol. 82, 109112. CrossRefGoogle Scholar
Arneri, E., Giannetti, G., Antolini, B., 1998, Age determination and growth of Venus verrucosa L. (Bivalvia: Veneridae) in the southern Adriatic and the Aegean Sea. Fish. Res. 38, 193198. CrossRefGoogle Scholar
Barbin, L., Boarini, I., Borasio, P.G., Barion, P., Fiorini, S., Rossi, R., Biondi, C., 2003, Nitric oxide-mediated arachidonic acid release from perifused Venus verrucosa oocytes. Gen. Comp. Endocrinol. 130, 215221. CrossRefGoogle Scholar
Bayne, B.L., 2004, Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve molluscs. Integr. Comp. Biol. 44, 425432. CrossRefGoogle ScholarPubMed
Belicka, L.L., Sokol, E.R., Hoch, J.M., Jaffé, R., Trexler, J.C., 2012, A molecular and stable isotopic approach to investigate algal and detrital energy pathways in a freshwater marsh. Wetlands 32, 531542. CrossRefGoogle Scholar
Bligh, E.G., Dyer, W.J., 1959, A rapid method of total lipid extraction and purification. Can J. Biochem. Physiol. 37, 911917 CrossRefGoogle ScholarPubMed
Blott, S.J., Pye, K., 2001, GRADISTAT: A grain size distribution and statistics package for the analysis of unconsolidated sediments. Earth Surf. Process. Landforms 26, 12371248 CrossRefGoogle Scholar
CNROP, 1993, Fisheries and stock evaluation in Mauritania: avenues for development and management. Report of the 3rd Working Group of CNROP, Nouadhibou, Mauritania. http://hdl.handle.net/1834/1246.
Cranford, P.J., Grant, J., 1990, Particle clearance and absorption of phytoplankton and detritus by the sea scallop Placopecten magellanicus (Gmelin). J. Exp. Mar. Biol. Ecol. 137, 105121. CrossRefGoogle Scholar
Dalsgaard, J., St John, M., Kattner, G., Muller-Navarra, D., Hagen, W., 2003, Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46, 225340. CrossRefGoogle ScholarPubMed
Dame R.F., 1996, Ecology of marine bivalves: an ecosystem approach, Boca Raton, CRC Press.
Dang, C., de Montaudouin, X., Gam, M., Paroissin, C., Bru, N., Caill-Milly, N., 2010, The Manila clam population in Arcachon Bay (SW France) : Can it be kept sustainable? J. Sea Res. 63, 108118. CrossRefGoogle Scholar
De Montaudouin, X., 1996, Factors involved in growth plasticity of cockles Cerastoderma edule (L), identified by field survey and transplant experiments. J. Sea Res. 36, 251265. CrossRefGoogle Scholar
Djabali F., Yahiaoui M., 1978, La praire (Venus verrucosa L.) en rade de Brest et en baie de Granville : biologie – production – exploitation. Thèse Université de Bretagne Occidentale, Brest.
El-Menif, N.T., Guezzi, Y., Lahbib, Y., Ramdani, M., Flower, R., 2008, Effects of biogenic concretions, epibionts, and endobionts on the relative growth of the clam Venus verrucosa in Bizerta Lagoon, Tunisia. J. Shellfish Res. 27, 10871092. CrossRefGoogle Scholar
Ezgeta-Balic, D., Najdek, M., Peharda, M., Blazina, M., 2012, Seasonal fatty acid profile analysis to trace origin of food sources of four commercially important bivalves. Aquaculture 334, 89100. CrossRefGoogle Scholar
Fredriksen, S., 2003, Food web studies in a Norwegian kelp forest based on stable isotope (δ 13C and δ 15N) analysis. Mar. Ecol. Prog. Ser. 260, 7181. CrossRefGoogle Scholar
Gaillard B., 2010, Gestion d’une espèce à haute valeur patrimoniale dans l’archipel des îles Chausey : rôles respectifs des contraintes environnementales et anthropiques dans la dynamique des populations de la praire Venus verrucosa (L., 1758). Gestion des écosystèmes marins et côtiers. Université du Littoral Côte d’Opale de Calais, USTL, Lille, Master 2 Pro
Gillmor, R.B., 1982, Assessment of intertidal bivalve growth and capacity adaptations in suspension-feeding bivalves. Mar. Biol. 68, 277286. CrossRefGoogle Scholar
Glover, E.A., Taylor, J.D., 2010, Needles and pins: acicular crystalline periostracal calcification in venerid bivalves (Bivalvia: Veneridae). J. Mollus. Stud. 76, 157179. CrossRefGoogle Scholar
Godet L., 2008, L’évaluation des besoins de conservation d’un patrimoine naturel littoral marin: l’exemple des estrans meubles de l’archipel de Chausey. Thèse, Muséum National d’Histoire Naturelle, Paris.
Godet, L., Toupoint, N., Fournier, J., Le Mao, P., Retiere, C., Olivier, F., 2009, Clam farmers and oystercatchers: effects of the degradation of Lanice conchilega beds by shellfish farming on the spatial distribution of shorebirds. Mar. Pollut. Bull. 58, 589595. CrossRefGoogle ScholarPubMed
Gollety, C., Riera, P., Davoult, D., 2010, Complexity of the food web structure of the Ascophylum nodosum zone evidenced by a δ 13C and δ 15N study. J. Sea Res. 64, 304312. CrossRefGoogle Scholar
Gosling E., 2003, Bivalve molluscs: Biology, Ecology and Culture, Oxford, Blackwell Publishing Ltd.
Gunsen, U., Aydin, A., Ozcan, A., 2008, Determination of the toxin profile of Venus gallina, Venus verrucosa and Cardium edule mussels in Turkey. Arch. Lebensmittelhyg. 59, 233238. Google Scholar
Higgins R.P., Thiel H., 1988, Introduction to the study of meiofauna, Washington, DC, Smithsonian Institution Press.
Jeffrey S.W., Mantoura R.F.C., Whright S.W., 1997, Phytoplankton pigments in oceanography: guidelines to modern methods, Paris, UNESCO.
Kelly, J.R., Scheibling, R.E., 2012, Fatty acids as dietary tracers in benthic food webs. Mar. Ecol. Prog. Ser. 446, 122. CrossRefGoogle Scholar
Lami, R., 1972, Florule algologique des Iles Chausey par Gontran Hamel. Bull. Lab. Marit. Dinard 1, 225241. Google Scholar
Le Berre S., Brigand L., 2011, La pêche à pied dans l’archipel de Chausey (France) : contribution à une analyse des politiques de gestion durable de l’estran à travers la prise en compte des activités récréatives. In: Tagliani F. (Ed) Insularité et développement durable, Brest, IRD, Coll. Objectifs Sud, pp.149–167.
Lorrain, A., Paulet, Y.M., Chauvaud, L., Savoye, N., Donval, A., Saout, C., 2002, Differential delta C-13 and delta N-15 signatures among scallop tissues: implications for ecology and physiology. J. Exp. Mar. Biol. Ecol. 275, 4761. CrossRefGoogle Scholar
McCutchan, J.H., Lewis, W.M., Kendall, C., McGrath, C.C., 2003, Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378390. CrossRefGoogle Scholar
Meyers, P.A., 1997, Organic geochemical proxies of paleoceanographic, paleolimnologic, and paleoclimatic processes. Org. Geochem. 27, 213250. CrossRefGoogle Scholar
Meziane, T., Tsuchiya, M., 2002, Organic matter in a subtropical mangrove-estuary subjected to wastewater discharge: Origin and utilisation by two macrozoobenthic species. J. Sea Res. 47, 111. CrossRefGoogle Scholar
Michener R.H., Kaufman L., 2007, Stable isotope ratios as tracers. In: Michener R.H., Lajtha K. (Eds.) Stable isotopes in ecology and environmental science. Blackwell, Malden, pp. 238–282.
Miller, R.J., Page, H.M., 2012, Kelp as a trophic resource for marine suspension feeders: a review of isotope-based evidence. Mar. Biol. 159, 13911402. CrossRefGoogle Scholar
Mortillaro, J.M., Abril, G., Moreira-Turcq, P., Sobrinho, R.L., Perez, M., Meziane, T., 2011, Fatty acid and stable isotope δ 13C and δ 15N signatures of particulate organic matter in the lower Amazon River: Seasonal contrasts and connectivity between floodplain lakes and the mainstem. Org. Geochem. 42, 11591168. CrossRefGoogle Scholar
Morton, B., Peharda, M., Petric, M., 2011, Functional morphology of Rocellaria dubia (Bivalvia: Gastrochaenidae) with new interpretations of crypt formation and adventitious tube construction, and a discussion of evolution within the family. Biol. J. Linn. Soc. 104, 786804. CrossRefGoogle Scholar
Nerot, C., Lorrain, A., Grall, J., Gillikin, D.P., Munaron, J.M., Le Bris, H., Paulet, Y.M., 2012, Stable isotope variations in benthic filter feeders across a large depth gradient on the continental shelf. Estuar. Coast. Shelf Sci. 96, 228235 CrossRefGoogle Scholar
Pasquale, V., Romano, V., Rupnik, M., Capuano, F., Bove, D., Aliberti, F., Krovacek, K., Dumontet, S., 2012, Occurrence of toxigenic Clostridium difficile in edible bivalve molluscs. Food Microbiol. 31, 309312. CrossRefGoogle ScholarPubMed
Pauly, D., Munro, J.L., 1984, Once more on the comparison of growth in fishes and invertebrates. Fishbyte 2, 2122 Google Scholar
Peharda, M., Ezgeta-Balic, D., Vrgoc, N., Isajlovic, I., Bogner, D., 2010, Description of bivalve community structure in the Croatian part of the Adriatic Sea - hydraulic dredge survey. Acta Adriat. 51, 141158. Google Scholar
Pernet, F., Gauthier-Clerc, S., Mayrand, É., 2007, Change in lipid composition in eastern oyster (Crassostrea virginica Gmelin) exposed to constant or fluctuating temperature regimes. Comp. Biochem. Physiol. 147, 557565. CrossRefGoogle ScholarPubMed
Peterson, B.J., Fry, B., 1987, Stable isotopes in ecosystem studies. Annu. Rev. Ecol. Syst. 18, 293320. CrossRefGoogle Scholar
Pitel M., Berthou P., Fifas S., 2001, Caractéristiques de dragues et pêcheries. Ifremer Rep., Brest.
Pitel-Roudaut M., Martin S., Fifas S., Huet J., Berthou P., 2006, Évaluation du stock de praires en rade de Brest. Ifremer Rep. Brest.
Poppe G.T., Goto Y., 1993, European seashells. Volume 2 (Scaphopoda, Bivalvia, Cephalopoda). Wiesbaden, Verlag Christa Hemmen.
Post, D.M., 2002, Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83, 703718. CrossRefGoogle Scholar
Quinn G.P., Keough M.J., 2002, Experimental design and data analysis for biologists, Cambridge, Cambridge University Press.
Richardson, C.A., Crisp, D.J., Runham, N.W., 1980, Factors influencing shell growth in Cerastoderma edule. Proc. R. Soc. Lond. B. Biol. 210, 513531. CrossRefGoogle Scholar
Riera, P., Stal, L., Nieuwenhuize, J., 2004, Utilization of food sources by invertebrates in a man-made intertidal ecosystem (Westerschelde, the Netherlands): a δ 13C and δ 15N study. J. Mar. Biol. Assoc. UK 84, 323326. CrossRefGoogle Scholar
Romeo, M., Gnassia-Barelli, M., 1988, Donax trunculus and Venus verrucosa as bioindicators of trace-metal concentrations in Mauritanian coastal waters. Mar. Biol. 99, 223227. CrossRefGoogle Scholar
Ronconi, R.A., Koopman, H.N., McKinstry, C.A.E., Wong, S.N.P., Westgate, A.J., 2010, Inter-annual variability in diet of non-breeding pelagic seabirds Puffinus spp. at migratory staging areas: evidence from stable isotopes and fatty acids. Mar. Ecol. Prog. Ser. 419, 267282. CrossRefGoogle Scholar
Royer, C., Thébault, J., Chauvaud, L., Olivier, F., 2013, Structural analysis and paleoenvironmental potential of dog cockle shells (Glycymeris glycymeris) in Brittany, northwest France. Palaeogeogr. Paleoclim. Paleoecol. 373, 123132. CrossRefGoogle Scholar
Rufino, M.M., Gaspar, M.B., Pereira, A.M., Maynou, F., Monteiro, C.C., 2010, Ecology of megabenthic bivalve communities from sandy beaches on the south coast of Portugal. Sci. Mar. 74, 163178. CrossRefGoogle Scholar
Siniscalchi, A., Cavallini, S., Sonetti, D., Sbrenna, G., Capuano, S., Barbin, L., Turolla, E., Rossi, R., 2004, Serotonergic neurotransmission in the bivalve Venus verrucosa (Veneridae): a neurochemical and immunohistochemical study of the visceral ganglion and gonads. Mar. Biol. 144, 12051212. CrossRefGoogle Scholar
Sokal R.R., Rohlf F.J., 1995, Biometry: The principles and practice of statistics in biological research. New York, 3rd edition, W.H. Freeman.
Thompson, R.J., 1984, Production, reproductive effort, reproductive value and reproductive cost in a population of the blue mussel Mytilus edulis from a subarctic environment. Mar. Ecol. Prog. Ser. 16, 249257. CrossRefGoogle Scholar
Tirado, C., Salas, C., Marquez, I., 2003, Reproduction of Venus verrucosa L., 1758 (Bivalvia: Veneridae) in the littoral of Malaga (southern Spain). Fish. Res. 63, 437445. CrossRefGoogle Scholar
Toupoint, N., Godet, L., Fournier, J., Retière, C., Olivier, F., 2008, Does Manila clam cultivation affect habitats of the engineer species Lanice conchilega (Pallas, 1766)? Mar. Pollut. Bull. 56, 14291438. CrossRefGoogle Scholar
Trigui El-Menif, N., Guezzi, Y., Le Pennec, M., Boumaiza, M., Le Pennec, G., 2005, Infestation of the clam Venus verrucosa by Sipunculoidea and the lithophagus bivalve, Gastrochaena dubia. Acta Adrat. 46, 8390. Google Scholar
Tucker M.J., Pitt E.G., 2001. Waves in Ocean Engineering. Elsevier Science.
Urban, H.J., 1994, Adaptations of six infaunal bivalve species of Chile: Coexistence resulting from differences in morphology, burrowing depth and substrate preference. Arch. Fish. Mar. Res. 42, 183193. Google Scholar
Vogel, S., 1984, Drag and flexibility in sessile organisms. Am. Zool. 24, 3744. CrossRefGoogle Scholar
Wildish D., Kristmanson D., 2005, Benthic suspension feeders and flow. New York, Cambridge University Press
Wildish, D.J., Saulnier, A.M., 1993, Hydrodynamic control of filtration in Placopecten magellanicus. J. Exp. Mar. Biol. Ecol. 174, 6582. CrossRefGoogle Scholar