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Bioaccumulation of essential metals (Co, Mn and Zn) in the king scallop Pecten maximus: seawater, food and sediment exposures

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Abstract

In order to understand the bioaccumulation of essential metals in filter-feeding mollusks living in soft sediments, the uptake and depuration kinetics of three elements (Co, Mn and Zn) were investigated in the king scallop Pecten maximus exposed via seawater, food, or sediment, using radiotracer techniques. The scallops were collected in April 2005 in the Pertuis Breton, France and acclimated to laboratory conditions for 8 weeks prior to the experimental exposures. Dissolved metals were efficiently bioconcentrated with mean concentration factors (CFs) ranging from 65 (Co) to 94 (Mn) after 7 days of exposure. Feeding experiments using microalgae Skeletonema costatum (diatom) or Isochrysis galbana (flagellate) showed that metal assimilation efficiency (AE) and retention (T b½) were strongly influenced by food source. For Co, AE was higher when ingested with I. galbana (29 vs. 4%), whereas Mn and Zn AE was higher for S. costatum (82 vs. 44% and 86 vs. 68%, respectively). Transfer factors (TFs) in P. maximus exposed to radiolabelled sediment were 3–4 orders of magnitude lower than CFs. Nevertheless, the fraction of sediment-bound metals that was taken up was efficiently absorbed in scallop tissues (>85%). Whatever the exposure pathway, metals were strongly retained in the kidneys of P. maximus. Due to poor determination of Mn biokinetics (and related parameters) in scallops exposed through sediment, the relative contribution of the three different pathways could be determined only for Co and Zn using a biodynamic model. The particulate pathway (i.e. food or sediment) appeared to be the main route for bioaccumulation of both metals in this scallop. In addition, even though P. maximus displayed different AEs for Co and Zn according to the food, results of the model were only slightly affected, if any, by change in the dietary parameters (AE and depuration rate constant, k e).

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References

  • Berthet B, Amiard JC, Amiard-Triquet C, Martoja R, Jeantet AY (1992) Bioaccumulation, toxicity and physico-chemical speciation of silver in bivalve molluscs: ecotoxicological and health consequences. Sci Total Environ 125:97–122

    Article  CAS  Google Scholar 

  • Bryan GW (1973) The occurence and seasonal variation of trace metals in the scallops Pecten maximus (L.) and Chlamys opercularis (L.). J Mar Biol Assoc UK 53:145–166

    Article  CAS  Google Scholar 

  • Bustamante P, Miramand P (2004) Interspecific and geographical variations of trace element concentrations in Pectinidae from European waters. Chemosphere 57:1355–1362

    Article  PubMed  CAS  Google Scholar 

  • Bustamante P, Miramand P (2005) Subcellular and body distributions of 17 trace elements in the variegated scallop Chlamys varia from the French coast of the Bay of Biscay. Sci Total Environ 337:59–73

    Article  PubMed  CAS  Google Scholar 

  • Bustamante P, Bertrand M, Boucaud-Camou E, Miramand P (2006) Subcellular distribution of Ag, Cd, Co, Cu, Fe, Mn, Pb and Zn in the digestive gland of the common cuttlefish sepia officinialis. J Shellfish Res 25:987–993

    Google Scholar 

  • Coombs TL (1972) The distribution of zinc in the oyster Ostrea edulis and its relation with enzymatic activity and to other metals. Mar Biol 12:170–178

    Article  CAS  Google Scholar 

  • Croft MT, Warren MJ, Smith AG (2006) Algae need their vitamins. Eukaryotic Cell 5:1175–1183

    Article  PubMed  CAS  Google Scholar 

  • Danis B, Cotret O, Teyssié JL, Fowler SW, Bustamante P, Warnau M (2003) Delineation of PCB uptake pathways in a benthic sea star using a radiolabelled congener. Mar Ecol Prog Ser 253:155–163

    Article  CAS  Google Scholar 

  • Danis B, Wantier P, Flammang R, Dutrieux S, Dubois P, Warnau M (2004) Contaminant levels in sediment and asteroids (Asterias rubens, Echinoderm) from the Belgian coast and Scheldt estuary: polychlorinated biphenyls and metals. Sci Total Environ 333:149–165

    Article  PubMed  CAS  Google Scholar 

  • Danis B, Bustamante P, Cotret O, Teyssié JL, Fowler SW, Warnau M (2005) Bioaccumulation of PCBs in the cuttlefish Sepia officinalis from sea water, sediment and food pathways. Environ Pollut 134:113–122

    Article  PubMed  CAS  Google Scholar 

  • Förstner U, Wittmann GT (1983) Marine pollution in the aquatic environment, 2nd edn. Springer, Berlin

    Google Scholar 

  • Fowler BA, Gould E (1988) Ultrastructural and biochemical studies of intracellular metal-binding patterns in kidney tubule cells of the scallop Placopecten magellanicus following prolonged exposure to cadmium or copper. Mar Biol 97:207–216

    Article  CAS  Google Scholar 

  • George SG, Pirie BJS, Coombs TL (1980) Isolation and elemental analysis of metal-rich granules from kidney of the scallop Pecten maximum (L.). J Exp Mar Biol Ecol 42:143–156

    Article  CAS  Google Scholar 

  • Gould E, Greig RA, Rusanowsky D, Marks BC (1985) Metal-exposed sea scallops, Placopecten magellanicus (Gmelin): a comparison of the effects and uptake of cadmium and copper. In: Vernberg FJ, Thurberg FP, Callabrese A, Vernberg WB (eds) Marine pollution and physiology, recent advances. University of South Carolina Press, Columbia, pp 157–186

    Google Scholar 

  • Hamilton EI (1994) The geochemistry of cobalt. SciTotal Environ 150:7–39

    Article  CAS  Google Scholar 

  • Hédouin L, Metian M, Teyssié JL, Fichez R, Warnau M (2009) Delineation of heavy metal contamination pathways (seawater, food and sediment) in tropical oysters from New Caledonia using radiotracer techniques. Mar Pollut Bull (in press)

  • IAEA (2004) Sediments distribution coefficients and concentration factors for biota in the marine environment. International Atomic Energy Agency, Vienna

    Google Scholar 

  • Lacoue-Labarthe T, Warnau M, Oberhänsli F, Teyssié JL, Kouéta N, Bustamante P (2008) Differential bioaccumulation behaviour of Ag and Cd during the early development of the cuttlefish Sepia officinalis. Aquat Toxicol 86:437–446

    Article  PubMed  CAS  Google Scholar 

  • Landrum PF, Lee H, Lydy MJ (1992) Toxicokinetics in aquatic systems: model comparisons and use in hazard assessment. Environ Toxicol Chem 11:1709–1725

    Article  CAS  Google Scholar 

  • Mauri M, Orlando E, Nigro M, Regoli F (1990) Heavy metals in the Antarctic scallop Adamussium colbecki. Mar Ecol Prog Ser 67:27–33

    Article  CAS  Google Scholar 

  • Metayer C, Amiard-Triquet C, Baud JP (1990) Variations inter-spécifiques de la bioaccumulation et de la toxicité de l’argent à l’égard de trois mollusques bivalves marins: species-related variations of silver bioaccumulation and toxicity to three marine bivalves. Water Res 24:995–1001

    Article  CAS  Google Scholar 

  • Metian M, Warnau M, Oberhänsli F, Teyssié JL, Bustamante (2007) Interspecific comparison of Cd bioaccumulation in European Pectinidae (Chlamys varia and Pecten maximus). J Exp Mar Biol Ecol 353:58–67

    Article  CAS  Google Scholar 

  • Metian M, Bustamante P, Cosson RP, Hédouin L, Warnau M (2008a) Investigation of Ag in the king scallop Pecten maximus using field and laboratory approaches. J Exp Mar Biol Ecol 367:53–60

    Article  CAS  Google Scholar 

  • Metian M, Bustamante P, Hédouin L, Warnau M (2008b) Accumulation of nine metals and one metalloid in the tropical scallop Comptopallium radula from coral reefs in New Caledonia. Environ Pollut 152:543–552

    Article  PubMed  CAS  Google Scholar 

  • Metian M, Bustamante P, Hédouin L, Oberhänsli F, Warnau M (2009) Delineation of heavy metal uptake pathways (seawater and food) in the variegated scallop Chlamys varia using radiotracer techniques. Mar Ecol Prog Ser 375:161–171

    Article  Google Scholar 

  • Mikulich LV, Tsikhon-Lukamina A (1981) Food of the scallop. Oceanology 21:633–635

    Google Scholar 

  • Nelson DA, Calabrese A, Nelson BA, Maclnnes JR, Wenzloff DR (1976) Biological effects of heavy metals on juvenile bay scallops, Argopecten irradians, in short term exposures. Bull Environ Contam Toxicol 16:275–282

    Article  PubMed  CAS  Google Scholar 

  • Ng TYT, Amiard-Triquet C, Rainbow PS, Amiard JC, Wang WX (2005) Physicochemical form of trace metals accumulated by phytoplancton and their assimilation by filter feeder. Mar Ecol Prog Ser 299:179–191

    Article  CAS  Google Scholar 

  • Nolan CV, Fowler SW, Teyssié JL (1992) Cobalt speciation and bioavailability in marine organisms. Mar Ecol Prog Ser 88:105–116

    Article  CAS  Google Scholar 

  • Pecquenat JE, Fowler SW, Small LF (1969) Estimates of the zinc requirements of marine organisms. J Fish Res Board Can 26:145–150

    Google Scholar 

  • Pesch GG, Steward NE, Pesch C (1979) Copper toxicity to the bay scallop (Argopecten irradians). Bull Environ Contam Toxicol 23:759–765

    Article  PubMed  CAS  Google Scholar 

  • Rainbow PS (2002) Trace metal concentrations in aquatic invertebrates: why and so what? Environ Pollut 120:497–507

    Article  PubMed  CAS  Google Scholar 

  • Reinfelder JR, Fisher NS (1991) The assimilation of elements ingested by marine copepods. Science 251:794–796

    Article  PubMed  CAS  Google Scholar 

  • Reinfelder JR, Wang WX, Luoma SN, Fisher NS (1997) Assimilation efficiencies and turnover rates of trace elements in marine bivalves: a comparison of oysters, clams and mussels. Mar Biol 129:443–452

    Article  CAS  Google Scholar 

  • Reinfelder JR, Fisher NS, Luoma SN, Nichols JW, Wang WX (1998) Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach. Sci Total Environ 219:117–135

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez y Baena AM, Miquel JC, Masqué P, Povinec P, La Rosa J (2006a) A single vs. double spike approach to improve the accuracy of 234Th measurements in small-volume seawater samples. Mar Chem 100:269–281

    Article  CAS  Google Scholar 

  • Rodriguez y Baena AM, Metian M, Teyssié JL, De Broyer C, Warnau M (2006b) Experimental evidence for 234Th bioaccumulation in three Antarctic crustaceans: potential implications for particle flux studies. Mar Chem 100:354–365

    Article  CAS  Google Scholar 

  • Shumway SE, Selvin R, Schick DF (1987) Food resources related to habitat in the scallop Placopecten magellanicus (Gmelin, 1791): a qualitative study. J Shellfish Res 6:89–95

    Google Scholar 

  • Simkiss K (1979) Metal ions in cells. Endeavour New Ser 3:2–6

    Article  CAS  Google Scholar 

  • Temara A, Ledent G, Warnau M, Paucot H, Jangoux M, Dubois P (1996) Experimental cadmium contamination of Asterias rubens (Echinodermata). Mar Ecol Prog Ser 140:83–90

    Article  CAS  Google Scholar 

  • Thomann RV (1981) Equilibrium model of fate of microcontaminants in diverse aquatic food chains. Can J Fish Aquat Sci 38:280–296

    Article  CAS  Google Scholar 

  • Thomann RV, Mahony JD, Mueller R (1995) Steady-state model of biota sediment accumulation factor for metals in two marine bivalves. Environ Toxicol Chem 14:1989–1998

    Article  CAS  Google Scholar 

  • Wang WX, Fisher NS (1999) Delineating metal accumulation pathways for marine invertebrates. Sci Total Environ 237(238):459–472

    Article  Google Scholar 

  • Warnau M, Teyssié JL, Fowler SW (1996) Biokinetics of selected heavy metals and radionuclides in the common Mediterranean echinoid Paracentrotus lividus: sea water and food exposures. Mar Ecol Prog Ser 141:83–94

    Article  CAS  Google Scholar 

  • Whicker FW, Schultz V (1982) Radioecology: nuclear energy and the environment. CRC Press, Florida

    Google Scholar 

  • White A, Handler P, Smith EL (1973) Principles of biochemistry. McGraw-Hill, New York

    Google Scholar 

  • Williams RJP (1981) Physico-chemical aspects of inorganic element transfer through membranes. Phil Trans Royal Soc B 294:57–74

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Authors are grateful to F. Oberhänsli and J.L. Teyssié (IAEA-MEL) for skilful technical assistance. We also thank the anonymous reviewers for critical review of the manuscript and fruitful suggestions. MW is an Honorary Senior Research Associate of the National Fund for Scientific Research (NFSR, Belgium) and holds a 2008–2009 Invited Expert position at LIENSs (CNRS-Université de La Rochelle) supported by the Conseil Régional de Poitou-Charente. This work was supported by the IAEA, the Conseil Général de la Charente-Maritime and the GIP Seine-Aval Programme. The IAEA is grateful for the support provided to its Marine Environment Laboratories by the Government of the Principality of Monaco. The experiments described herein comply with the current laws of the Principality of Monaco and France.

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Authors and Affiliations

  1. International Atomic Energy Agency-Marine Environment Laboratories (lAEA-MEL), 4 Quai Antoine Ier, 98000, Principality of Monaco, Monaco

    Marc Metian, Michel Warnau & Laetitia Hédouin

  2. Littoral, Environnement et Sociétés (LIENSs), UMR 6250, CNRS-Université de La Rochelle, 2 rue Olympe de Gouges, 17042, La Rochelle Cedex 01, France

    Marc Metian, Michel Warnau, Laetitia Hédouin & Paco Bustamante

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  1. Marc Metian
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  2. Michel Warnau
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  3. Laetitia Hédouin
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  4. Paco Bustamante
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Correspondence to Michel Warnau.

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Communicated by J. P. Grassle.

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Metian, M., Warnau, M., Hédouin, L. et al. Bioaccumulation of essential metals (Co, Mn and Zn) in the king scallop Pecten maximus: seawater, food and sediment exposures. Mar Biol 156, 2063–2075 (2009). https://doi.org/10.1007/s00227-009-1237-7

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  • DOI: https://doi.org/10.1007/s00227-009-1237-7

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