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Stable isotopes (δ13C, δ15N) and modelling as tools to estimate the trophic ecology of cultivated oysters in two contrasting environments

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Abstract

Food sources for cultivated marine bivalves generally are not well identified, although they are essential for a better understanding of coastal ecosystems and for the sustainability of shellfish farming activities. In addition to phytoplankton, other organic matter sources (OMS), such as microphytobenthos and detritus (of terrestrial or marine origins), can contribute significantly to the growth of marine bivalves. The aim of this study was to identify the potential food sources and to estimate their contributions to the growth of the Pacific oyster (Crassostrea gigas) in two contrasting trophic environments of Normandy (France): the Baie des Veys (BDV) and the Lingreville area (LIN). Two sites were studied in the BDV area (BDV-S and BDV-N) and one in the LIN area. To estimate the contribution of each type of OMS, we used a combination of stable natural isotope composition (δ13C, δ15N) analysis of OMS and oyster tissue together with a modelling exercise. Field sampling was conducted every 2 months over 1 year. The sampled sources were suspended particulate organic matter from marine (PhyOM) and terrestrial (TOM) origins, microphytobenthos (MPB), detrital organic matter from the superficial sediment (SOM), and macroalgae (Ulva sp., ULV). A statistical mixing model coupled to a bioenergetic model was used to calculate the contributions of each different source at different seasons. Results showed that isotopic composition of the animal flesh varied with respect to the potential OMS over the year within each ecosystem. Significant differences were also observed among the three locations. For instance, the δ13C and δ15N values of the oysters ranged from −20.0 to −19.1‰ and from 6.9 to 10.8‰ at BDV-S, from −19.4 to −18.1‰ and from 6.4 to 10.0‰ at BDV-N, and from −21.8 to −19.4‰ and from 6.3 to 8.3‰ at LIN. The contributions of the different sources to oyster growth differed depending on the ecosystem and on the period of the year. Phytoplankton (PhyOM) predominated as the principal food source for oysters (particularly in the LIN location). MPB, TOM, and ULV detritus also possibly contributed to oysters’ diet during summer and autumn at the BDV-S and BDV-N sites. SOM was not considered an OMS because it was already a mix of the other four OMS, but rather a trophic reservoir that potentially mirrored the trophic functioning of marine ecosystems.

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References

  • Aminot A, Kérouel R (2004) Hydrologie des écosystèmes marins paramètres et analyses. Editions IFREMER, Plouzané, Finistère

  • Andrews J, Greenaway A, Dennis P (1998) Combined carbon isotope and C/N ratios as indicators of source and fate of organic matter in a poorly flushed, tropical estuary: Hunts bay, Kingston Harbour, Jamaica. Estuar Coast Shelf Sci 46:743–756

    Article  CAS  Google Scholar 

  • Barillé L, Prou J, Héral M, Razet D (1997) Effects of high natural seston concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg). J Exp Mar Biol Ecol 212:149–172

    Article  Google Scholar 

  • Behringer DC, Butler MJ (2006) Density-dependent population dynamics in juvenile Panulirus argus (Latreille): the impact of artificial density enhancement. J Exp Mar Biol Ecol 334:84–95

    Article  Google Scholar 

  • Bianchi T, Argyrou M (1997) Temporal and spatial dynamics of particulate organic carbon in the lake Pontchartrain Estuary, Southeast Louisiana, USA. Estuar Coast Shelf Sci 45:557–569

    Article  CAS  Google Scholar 

  • Blanchard G, Chretiennot-Dinet MJ, Dinet A, Robert JM (1988) Méthode simplifiée pour l’extraction du microphytobenthos des sédiments marins par le gel de silice Ludox. C R Acad Sci Paris, Série III 307:569–576

    Google Scholar 

  • Bougrier S, Hawkins AJS, Héral M (1997) Preingestive selection of different microalgal mixture in Crassostrea gigas and Mytilus edulis, analysed by flow cytometry. Aquaculture 150:123–134

    Article  Google Scholar 

  • Cognie B, Barillé L (1999) Does bivalve mucus favour the growth of their main food source, microalgae? Oceanol Acta 22:441–450

    Article  Google Scholar 

  • Costil K, Royer J, Ropert M, Soletchnik P, Mathieu M (2005) Spatio-temporal variations in biological performances and summer mortality of the oyster Crassostrea gigas in Normandy (France). Helgol Mar Res 59:286–300

    Article  Google Scholar 

  • Crosby MP, Newell RIE (1990) Bacterial mediation in the utilization of carbon and nitrogen from detrital complexes by Crassostrea virginica. Limnol Oceanogr 35:625–639

    Article  CAS  Google Scholar 

  • Currin CA, Newell SY, Paerl HW (1995) The role of standing dead Spartina alterniflora and benthic microalgae in salt-marsh food webs: considerations based on multiple stable-isotope analysis. Mar Ecol Prog Ser 121:99–116

    Article  Google Scholar 

  • Dame RF, Prins T (1998) Bivalve carrying capacity in coastal ecosystems. Aquat Ecol 31:409–421

    Article  Google Scholar 

  • de Jonge VN, Colijn F (1994) Dynamics of microphytobenthos biomass in the Ems estuary. Mar Ecol Prog Ser 104:185–196

    Article  Google Scholar 

  • Deegan LA, Garritt RH (1997) Evidence for spatial variability in estuarine food webs. Mar Ecol Prog Ser 147:31–47

    Article  Google Scholar 

  • Doi H, Matsumasa M, Toya T, Satoh N, Mizota C, Maki Y, Kikuchi E (2005) Spatial shifts in food sources for macrozoobenthos in an estuarine ecosystem: carbon and nitrogen stable isotope analyses. Estuar Coast Shelf Sci 64:316–322

    Article  Google Scholar 

  • Dubois S, Orvain F, Marín Leal JC, Ropert M, Lefebvre S (2007a) Small-scale spatial variability of food partitioning between cultivated oysters and associated suspension-feeding species, as revealed by stable isotopes. Mar Ecol Prog Ser 336:151–160

    Article  CAS  Google Scholar 

  • Dubois S, Blin JL, Bouchaud B, Lefebvre S (2007b) Isotope trophic step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems. J Exp Mar Biol Ecol 351:121–128

    Article  Google Scholar 

  • Dupuy C, Vaquer A, Lam-Höai T, Rougier C, Mazouni N, Lautier J, Collos Y, Le Gall S (2000) Feeding rate of the Crassostrea gigas in a natural planktonic community of the Mediterranean Thau Lagoon. Mar Ecol Prog Ser 205:171–184

    Article  Google Scholar 

  • Franco-Nava MA, Blancheton JP, Deviller G, Le-Gall JY (2004) Particulate matter dynamics and transformations in a recirculating aquaculture system: application of stable isotope tracers in seabass rearing. Aquac Eng 31:135–155

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Gaye-Siessegger J, Focken U, Muetzel S, Abel H, Becker K (2004) Feeding level and individual metabolic rate affect δ13C and δ15N values in carp: implications for food web studies. Oecologia 138:175–183

    Article  Google Scholar 

  • Gorokhova E, Hansson S (1999) An experimental study on variations in stable isotope carbon and nitrogen isotope fractionation during growth of Mysis mixta and Neomysis integer. Can J Fish Aquat Sci 56:2203–2210

    Article  Google Scholar 

  • Graham M, Eaves M, Farmer J, Dobson J, Fallick A (2001) A study of carbon and nitrogen stable isotope and elemental ratios as potential indicators of source and fate of organic matter in sediments of the Forth estuary, Scotland. Estuar Coast Shelf Sci 52:375–380

    Article  CAS  Google Scholar 

  • Gu B, Schelske CL, Brenner M (1996) Relationship between sediment and plankton isotope ratios (δ13C and δ15N) and primary productivity in Florida lakes. Can J Fish Aquat Sci 53:875–883

    Article  CAS  Google Scholar 

  • Harvey C, Hanson P, Essington T, Brown P, Kitchell J (2002) Using bioenergetics models to predict stable isotope ratios in fishes. Can J Fish Aquat Sci 59:115–124

    Article  Google Scholar 

  • Herman PMJ, Middelburg JJ, van de Koppel J, Heip CHR (1999) Ecology of estuarine macrobenthos. Adv Ecol Res 29:195–240

    Article  Google Scholar 

  • Herman PMJ, Middelburg JJ, Widdows J, Lucas CH, Heip CHR (2000) Stable isotopes as trophic tracers: combining field sampling and manipulative labelling of food resources for macrobenthos. Mar Ecol Prog Ser 204:79–92

    Article  CAS  Google Scholar 

  • Herzka SZ (2005) Assessing connectivity of estuarine fishes based on stable isotope ratio analysis. Estuar Coast Shelf Sci 64:58–69

    Article  Google Scholar 

  • Hsieh HL, Kao WY, Chen CP, Liu PJ (2000) Detrital flows through the feeding pathway of the oyster (Crassostrea gigas) in a tropical shallow lagoon: δ13C signals. Mar Biol 136:677–684

    Article  Google Scholar 

  • Josefson AB, Forbes TL, Rosenberg R (2002) Fate of phytodetritus in marine sediments: functional importance of macrofaunal community. Mar Ecol Prog Ser 230:71–85

    Article  Google Scholar 

  • Jouenne F, Lefebvre S, Véron B, Lagadeuc Y (2007) Phytoplankton community structure and primary production in small intertidal estuarine-bay ecosystem (eastern English Channel, France). Mar Biol 151:805–825

    Article  Google Scholar 

  • Kang CK, Sauriau PG, Richard P, Blanchard G (1999) Food sources of the infaunal suspension-feeding bivalve Cerastoderma edule in a muddy sandflat of Marennes-Oléron bay, as determined by analyses of carbon and nitrogen stable isotopes. Mar Ecol Prog Ser 187:147–158

    Article  Google Scholar 

  • Kang CK, Lee YW, Choy EJ, Shin JK, Seo IS, Hong JS (2006) Microphytobenthos seasonality determines growth and reproduction in intertidal bivalves. Mar Ecol Prog Ser 315:113–127

    Article  Google Scholar 

  • Langdon CJ, Newell RIE (1990) Utilization of detritus and bacteria as food sources by two bivalve suspension-feeders, the oyster Crassostrea virginica the mussel Geukensia demissa. Mar Ecol Prog Ser 58:299–310

    Article  Google Scholar 

  • Lorrain A, Savoye N, Chauvaud L, Paulet YM, Naulet N (2003) Decarbonatation and preservation method for the analysis of organic C and N contents and stable isotope ratios of low-carbonated suspended particulate material. Anal Chim Acta 491:125–133

    Article  CAS  Google Scholar 

  • Lundsgaard C, Olesen M (1997) The origin of sedimenting detrital matter in a coastal system. Limnol Oceanogr 42:1001–1005

    Article  Google Scholar 

  • Maksymowska D, Richard P, Piekarek-Jankowska H, Piera P (2000) Chemical and isotopic composition of the organic matter sources in the gulf of Gdansk (Southern Baltic Sea). Estuar Coast Shelf Sci 51:585–598

    Article  Google Scholar 

  • McCallister SJ, Bauer J, Ducklow H, Canuel E (2006) Sources of estuarine dissolved and particulate organic matter: a multi-tracer approach. Org Geochem 37:454–468

    Article  CAS  Google Scholar 

  • McCutchan JH, Lewis WM, Kendhall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Middelburg JJ, Nieuwenhuize J (1998) Carbon and nitrogen stable isotopes in suspended matter and sediments from the Schelde Estuary. Mar Chem 60:217–225

    Article  CAS  Google Scholar 

  • Miles A, Sundbäck K (2000) Diel variation in microphytobenthos productivity in areas of different tidal amplitude. Mar Ecol Prog Ser 205:11–22

    Article  Google Scholar 

  • Orvain F, Sauriau PG, Le Hir P (2003) A model of fluff layer erosion and subsequent bed erosion in the presence of the bioturbator, Hydrobia ulvae. J Mar Res 61:823–851

    Article  Google Scholar 

  • Page HM, Lastra M (2003) Diet of intertidal bivalves in the Ría de Arosa (NW Spain): evidence from stable C and N isotope analysis. Mar Biol 143:519–532

    Article  CAS  Google Scholar 

  • Paulet YM, Lorrain A, Richard J, Pouvreau S (2006) Experimental shift in diet δ13C: a potential tool for ecophysiological studies in marine bivalves. Org Geochem 37:1359–1370

    Article  CAS  Google Scholar 

  • Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269

    Article  Google Scholar 

  • Piola RF, Moore SK, Suthers IM (2006) Carbon and nitrogen stable isotope analysis of three types of oyster tissue in an impacted estuary. Estuar Coast Shelf Sci 66:255–266

    Article  Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    Article  Google Scholar 

  • Pouvreau S, Bourles Y, Lefebvre S, Gangnery A, Alunno-Bruscia M (2006) Application of a dynamic energy budget model to the Pacific oyster, Crassostrea gigas, reared under various environmental conditions. J Sea Res 56:156–167

    Article  Google Scholar 

  • Press WH, Teukolsky SA, Vetterling WT (2003) Numerical recipes in Fortran 77: the art of scientific computing. Cambridge University Press, London

    Google Scholar 

  • Pruell RJ, Taplin BK, Lake JL, Jayaraman S (2006) Nitrogen isotope ratios in estuarine biota collected along a nutrient gradient in Narragansett Bay, Rhode Island, USA. Mar Pollut Bull 52:612–620

    Article  CAS  Google Scholar 

  • Richard P, Riera P, Galois R (1997) Temporal variations in the chemical and carbon isotope compositions of marine and terrestrial organic inputs in the bay of Marennes-Oléron, France. J Coast Res 13:879–889

    Google Scholar 

  • Riera P, Richard P (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oléron. Estuar Coast Shelf Sci 42:347–360

    Article  Google Scholar 

  • Riera P, Richard P (1997) Temporal variation of δ13C in particulate organic matter and oyster Crassostrea gigas in Marennes-Oléron bay (France): effect of freshwater inflow. Mar Ecol Prog Ser 147:105–115

    Article  Google Scholar 

  • Riera P, Stal L, Nieuwenhuize J, Richard P, Blanchard G, Gentil F (1999) Determination of food sources for benthic invertebrates in a salt marsh (Aiguillon bay, France) by carbon and nitrogen stable isotopes: importance of locally produced sources. Mar Ecol Prog Ser 187:301–307

    Article  CAS  Google Scholar 

  • Ryba S, Burgess R (2002) Effects of sample preparation on the measurement of organic carbon, hydrogen, nitrogen, sulfur, and oxygen concentrations in marine sediments. Chemosphere 48:139–147

    Article  CAS  Google Scholar 

  • Savoye N, Aminot A, Tréguer P, Fontugne M, Naulet N, Kérouel R (2003) Dynamics of particulate organic matter δ15N and δ13C during spring phytoplankton blooms in a macrotidal ecosystem (bay of Seine, France). Mar Ecol Prog Ser 255:27–41

    Article  CAS  Google Scholar 

  • Scheiner SM (1993) MANOVA Multiple response variable and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, London, pp 99–115

    Google Scholar 

  • Schröder-Adams C (2006) Estuaries of the past and present: a biofacies perspective. Sediment Geol 190:289–298

    Article  Google Scholar 

  • Sponheimer M, Robinson T, Ayliffe L, Passey B, Roeder B, Shipley L, Lopez E, Cerling T, Dearing D, Ehleringer J (2003) An experimental study of carbon-isotope fractionation between diet, hair, and feces of mammalian herbivores. Can J Zool 81:871–876

    Article  CAS  Google Scholar 

  • Usui T, Nagao S, Yamamoto M, Suzuki K, Kudo I, Montani S, Noda A, Minagawa M (2006) Distribution and sources of organic matter in surficial sediments on the shelf and slope off Tokachi, western North Pacific, inferred from C and N stable isotopes and C/N ratios. Mar Chem 98:241–259

    Article  CAS  Google Scholar 

  • Vizzini S, Mazzola A (2003) Seasonal variations in the stable carbon and nitrogen isotope ratios (13C/12C and 15N/14N) of primary producers and consumers in a western Mediterranean coastal lagoon. Mar Biol 142:1009–1018

    Article  CAS  Google Scholar 

  • Vizzini S, Mazzola A (2006) Sources and transfer of organic matter in food webs of a Mediterranean coastal environment: evidence for spatial variability. Estuar Coast Shelf Sci 66:459–467

    Article  Google Scholar 

  • Von Ende CN (1993) Repeated measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, London, pp 99–115

    Google Scholar 

  • Ward JE, Levinton JS, Shumway SE, Cucci T (1998) Particle sorting in bivalves: in vivo determination of the pallial organs of selection. Mar Biol 131:283–292

    Article  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • Wysocki LA, Bianchi TS, Powell RT, Reuss N (2006) Spatial variability in the coupling of organic carbon, nutrients, and phytoplankton pigments in surface waters and sediments of the Mississippi River plume. Estuar Coast Shelf Sci 69:47–63

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Regional Council of Basse Normandie, the Agence de l’Eau Seine-Normandie, DIREN/DRAM/IFOP and Universidad del Zulia (Venezuela) in the field of the POMOYSTER program. The authors would like to thank SMEL, IFREMER, CREC, and E. Leroullier for their technical assistance, and also Sea Pen Scientific Writing LLC for editorial assistance. Finally, we would like to thank the comments of three anonymous reviewers who helped in improving the manuscript.

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Correspondence to Sébastien Lefebvre.

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Communicated by S.A. Poulet.

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Marín Leal, J.C., Dubois, S., Orvain, F. et al. Stable isotopes (δ13C, δ15N) and modelling as tools to estimate the trophic ecology of cultivated oysters in two contrasting environments. Mar Biol 153, 673–688 (2008). https://doi.org/10.1007/s00227-007-0841-7

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