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High contribution of the particulate uptake pathway to metal bioaccumulation in the tropical marine clam Gafrarium pectinatum

  • Aquatic organisms and biological responses to assess water contamination and ecotoxicity
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Abstract

The clam Gafrarium pectinatum was investigated to assess its usefulness as a bioindicator species of metal mining contamination in the New Caledonia lagoon. The uptake and depuration kinetics of Ag, Cd, Co, Cr, and Zn were determined following exposures via seawater, sediment, and food using highly sensitive radiotracer techniques (110mAg, 109Cd, 51Cr, 57Co, and 65Zn). When the clams were exposed to dissolved metals, Co, Zn, and Ag were readily incorporated in their tissues (concentration factors (CF) ranging from 181 to 4982 after 28 days of exposure) and all metals were strongly retained (biological half-lives always >2 months). The estimated transfer factor (TF) in clam tissues after a 35-day sediment exposure was 1 to 4 orders of magnitude lower than the estimated CF, indicating a lower bioavailability of sediment-bound metals than dissolved ones. Once incorporated, metals taken up from sediment and seawater were retained longer than metals ingested with food, indicating that the uptake pathway influences the storage processes of metals in clam tissues. Compilation of our data into a global bioaccumulation model indicated that, except for Ag that essentially originated from food (92%), sediment was the main source of metal bioaccumulation in the clam (more than 80%). These results highlight that bioaccumulation processes strongly depend from one metal to the other. The overall efficient bioaccumulation and retention capacities of the clam G. pectinatum confirm its usefulness as a bioindicator species that can provide time-integrated information about ambient contamination levels in the tropical marine coastal environment.

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References

  • Ambatsian P, Fernex F, Bernat M, Parron C, Lecolle J (1997) High metal inputs to closed seas: the New Caledonian lagoon. J Geochem Explor 59(1):59–74

  • Berthet B, Amiard J-C, Amiard-Triquet C et al (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 

  • Bird ECF, Dubois JP, Iltis JA (1984) The impacts of opencast mining on the rivers and coasts of New Caledonia. The United Nations University, Tokyo, p 53

  • Bonnet X, Briand MJ, Brischoux F et al (2014) Anguilliform fish reveal large scale contamination by mine trace elements in the coral reefs of New Caledonia. Sci Total Environ 470–471:876–882. doi:10.1016/j.scitotenv.2013.10.027

    Article  Google Scholar 

  • Borovicka J, Randa Z, Jelínek E et al (2007) Hyperaccumulation of silver by Amanita strobiliformis and related species of the section Lepidella. Mycol Res 111:1339–1344. doi:10.1016/j.mycres.2007.08.015

    Article  CAS  Google Scholar 

  • Boyden CR (1977) Effect of size upon metal content of shellfish. J Mar Biol Assoc United Kingdom 57:675–714

    Article  CAS  Google Scholar 

  • Bruland KD (1983) Trace elements in seawater. In: Chester R (ed) Riley JP. Chem. Oceanogr. Academic Press, London, pp 157–201

    Google Scholar 

  • Cheung KH, Gu J-D (2003) Reduction of chromate (CrO42-) by an enrichment consortium and an isolate of marine sulfate-reducing bacteria. Chemosphere 52:1523–1529

    Article  CAS  Google Scholar 

  • Chong K, Wang W-X (2000a) Assimilation of cadmium, chromium and zinc by the green mussel Perna viridis and the clam Ruditapes philippinarum. Environ Toxicol Chem 19:1660–1667

    Article  CAS  Google Scholar 

  • Chong K, Wang W-X (2000b) Bioavailability of sediment-bound Cd, Cr and Zn to the green mussel Perna viridis and the Manila clam Ruditapes philippinarum. J Exp Mar Bio Ecol 255:75–92

    Article  CAS  Google Scholar 

  • Dalvi A, Bacon W, Osborne R (2004) The past and the future of nickel laterites

  • Decho AW, Luoma SN (1991) Time-courses in the retention of food material in the bivalves Potamocorbula amurensis and Macoma balthica: significance to the absorption of carbon and chromium. Mar Ecol Prog Ser 78:303–314

    Article  CAS  Google Scholar 

  • Gissi F, Stauber JL, Binet MT et al (2016) A review of nickel toxicity to marine and estuarine tropical biota with particular reference to the South East Asian and Melanesian region. Environ Pollut 218:1308–1323. doi:10.1016/j.envpol.2016.08.089

    Article  CAS  Google Scholar 

  • Greger M (2004) Metal availability, uptake, transport and accumulation in plants. In: MNV P (ed) Heavy met. stress plants from biomol. to ecosyst, 2nd edn. Springer, Berlin, pp 1–27

    Google Scholar 

  • Griscom SB, Fisher NS, Luoma SN (2000) Geochemical influences on assimilation of sediment-bound metals in clams and mussels. Environ Sci Technol 34:91–99

    Article  CAS  Google Scholar 

  • Griscom SB, Fisher NS, Aller RC, Lee BG (2002a) Effects of gut chemistry in marine bivalves on the assimilation of metals from ingested sediment particles. J Mar Res 60:101–120

    Article  Google Scholar 

  • Griscom SB, Fisher NS, Luoma SN (2002b) Kinetic modeling of Ag, Cd and Co bioaccumulation in the clam Macoma balthica: quantifying dietary and dissolved sources. Mar Ecol Prog Ser 240:127–141

    Article  CAS  Google Scholar 

  • Hansen DJ, Berry WJ, Mahony JD et al (1996) Predicting the toxicity of metal-contaminated field sediments using interstitial concentration of metals and acid-volatile sulfide normalizations. Environ Toxicol Chem 15:2080–2094

    Article  CAS  Google Scholar 

  • Hédouin L, Metian M, Teyssié J-L et al (2006) Allometric relationships in the bioconcentration of heavy metals by the edible tropical clam Gafrarium tumidum. Sci Total Environ 366:154–163

    Article  Google Scholar 

  • Hédouin L, Pringault O, Metian M et al (2007) Nickel bioaccumulation in bivalves from the New Caledonia lagoon: seawater and food exposure. Chemosphere 66:1449–1457

    Article  Google Scholar 

  • Hédouin L, Bustamante P, Churlaud C et al (2008a) Trends in concentrations of selected metalloid and metals in two bivalves from the coral reefs in the SW lagoon of New Caledonia. Ecotoxicol Environ Saf 72:372–381

    Article  Google Scholar 

  • Hédouin L, Bustamante P, Fichez R, Warnau M (2008b) The tropical brown alga Lobophora variegata as a bioindicator of mining contamination in the New Caledonia lagoon: a field transplantation study. Mar Environ Res 66:438–444

    Article  Google Scholar 

  • Hédouin L, Gomez Batista M, Metian M et al (2010a) Metal and metalloid bioconcentration capacity of two tropical bivalves for monitoring the impact of land-based mining activities in the New Caledonia lagoon. Mar Pollut Bull 61:554–567

    Article  Google Scholar 

  • Hédouin L, Metian M, Lacoue-Labarthe T et al (2010b) Influence of food on the assimilation of selected metals in tropical bivalves from the New Caledonia lagoon: qualitative and quantitative aspects. Mar Pollut Bull 61:568–575

    Article  Google Scholar 

  • Hédouin L, Metian M, Teyssié J-L et al (2010c) Delineation of heavy metal contamination pathways (seawater, food and sediment) in tropical oysters from New Caledonia using radiotracer techniques. Mar Pollut Bull 61:542–553. doi:10.1016/j.marpolbul.2010.06.037

    Article  Google Scholar 

  • Hédouin L, Pringault O, Bustamante P et al (2011) Validation of two tropical marine bivalves as bioindicators of mining contamination in the New Caledonia lagoon: transplantation experiments. Water Res 45:483–496

    Article  Google Scholar 

  • Hédouin L, Metian M, Teyssié JL et al (2016) Bioaccumulation of 63Ni in the scleractinian coral Stylophora pistillata and isolated Symbiodinium using radiotracer techniques. Chemosphere 156:420–427

  • Howe PL, Reichelt-Brushett AJ, Clark MW (2014) Effects of Cd, Co, Cu, Ni and Zn on asexual reproduction and early development of the tropical sea anemone Aiptasia pulchella. Ecotoxicology 23:1593–1606. doi:10.1007/s10646-014-1299-2

    Article  CAS  Google Scholar 

  • IAEA (2004) Sediments distribution coefficients and concentration factors for biota in the marine environment. International Atomic Energy Agency (IAEA), Vienna, Austria 95 p

    Google Scholar 

  • Jaffré T, Pillon Y, Thomine S, Merlot S (2013) The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Front Plant Sci 4:279. doi:10.3389/fpls.2013.00279

    Article  Google Scholar 

  • Labrosse P, Fichez R, Farman R, Adams T (2000) New Caledonia. In: Sheppard CRC (ed) Seas Millenn. An Environ. Eval, Pergamon, Amsterdam, pp 723–736

    Google Scholar 

  • Laganier R (1991) Erosion, transport and sedimentation processes associated with open-coast mining in New Caledonia: interac- tions with weather and climate. ORSTOM, South Pacific environments: interactions with weather and climate, New Zealand;  p 83–5

  • 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 

  • Lee BG, Luoma SN (1998) Influence of microalgal biomass on absorption efficiency of Cd, Cr and Zn by two bivalves from San Francisco Bay. Limnol Oceanogr 43:1455–1466

    Article  CAS  Google Scholar 

  • Luoma SN (1989) Can we determine the biological availability of sediment-bound trace elements? Hydrobiologia 176(177):379–396

    Article  Google Scholar 

  • Mayer LM, Chen Z, Findlay RH et al (1996) Bioavailability of sedimentary contaminants subject to deposit-feeder digestion. Environ Sci Technol 30:2641–2645

    Article  CAS  Google Scholar 

  • Metian M, Warnau M (2008) The tropical brown alga Lobophora variegata: a prospective bioindicator for Ag contamination in tropical coastal waters. Bull Environ Contam Toxicol 81:455–458

    Article  CAS  Google Scholar 

  • Metian M, Hédouin L, Barbot C et al (2005) Use of radiotracer techniques to study subcellular distribution of metals and radionuclides in bivalves from the Noumea lagoon, New Caledonia. Bull Environ Contam Toxicol 75:89–93

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Metian M, Bustamante P, Cosson RP et al (2008a) Investigation of Ag in the king scallop Pecten maximus using field and laboratory approaches. J Exp Mar Bio 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  CAS  Google Scholar 

  • Metian M, Hédouin L, Giron E et al (2008c) The brown alga Lobophora variegata, a bioindicator species for surveying metal contamination in tropical marine environments. J Exp Mar Bio Ecol 362:49–54

    Article  CAS  Google Scholar 

  • Metian M, Bustamante P, Hédouin L et al (2009a) 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 

  • Metian M, Hédouin L, Warnau M, Bustamante P (2009b) Bioaccumulation kinetics of essential metals (Co, Mn and Zn) in the king scallop Pecten maximus: relative contribution of seawater, food and sediment pathways. Mar Biol 156:2063–2075

    Article  CAS  Google Scholar 

  • Metian M, Hédouin L, Eltayeb MM et al (2010) Metal and metalloid bioaccumulation in the Pacific blue shrimp Litopenaeus stylirostris (Stimpson) from New Caledonia: laboratory and field studies. Mar Pollut Bull 61:576–584. doi:10.1016/j.marpolbul.2010.06.035

    Article  CAS  Google Scholar 

  • Metian M, Warnau M, Chouvelon T et al (2013) Trace element bioaccumulation in reef fish from New Caledonia: influence of trophic groups and risk assessment for consumers. Mar Environ Res 87–88:26–36. doi:10.1016/j.marenvres.2013.03.001

    Article  Google Scholar 

  • Ng TY-T, Wang W-X (2004) Detoxification and effects of Ag, Cd, and Zn pre-exposure on metal uptake kinetics in the clam Ruditapes philippinarum. Mar Ecol Prog Ser 268:161–172

    Article  CAS  Google Scholar 

  • Ratte HT (1999) Bioaccumulation and toxicity of silver compounds: a review. Environ Toxicol Chem 18:89–108

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Reinfelder JR, Fisher NS (1994) The assimilation of elements ingested by marine planktonic bivalve larvae. Limnol Oceanogr 39:12–20

    Article  CAS  Google Scholar 

  • Reinfelder J, Wang W-X, Luoma SN, Fisher NS (1997) Assimilation efficencies 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 et al (1998) Trace element trophic transfer in aquatic organisms: a critique of the kinetic model approach. Sci Total Environ 219:117–135

    Article  CAS  Google Scholar 

  • Rodriguez y Baena AM, Metian M, Teyssié J-L et al (2006) Experimental evidence for 234Th bioaccumulation in three Antarctic crustaceans: potential implications for particle flux studies. Mar Chem 100:354–365. doi:10.1016/j.marchem.2005.10.022

    Article  CAS  Google Scholar 

  • Sañudo-Wilhelmy SA, Flegal R (1992) Anthropogenic silver in the southern California bight: a new tracer of sewage in coastal waters. Environ Sci Technol 26:2147–2151

    Article  Google Scholar 

  • Selck H, Forbes VE, Forbes TL (1998) Toxicity and toxicokinetics of cadmium in Capitella sp. I: relative importance of water and sediment as routes of cadmium uptake. Mar Ecol Prog Ser 164:167–178

    Article  CAS  Google Scholar 

  • Shanmugam P, Neelamani S, Ahn YH et al (2007) Assessment of the levels of coastal marine pollution of Chennai city, Southern India. Water Resour Manag 21:1187–1206. doi:10.1007/s11269-006-9075-6

    Article  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 W-X, Fisher NS (1996) Assimilation of trace elements and carbon by the mussel Mytilus edulis: effects of food composition. Limnol Oceanogr 41:197–207

    Article  CAS  Google Scholar 

  • Wang W-X, Fisher NS (1999) Assimilation efficiencies of chemical contaminants in aquatic invertebrates: a synthesis. Environ Toxicol Chem 18:2034–2045

    Article  CAS  Google Scholar 

  • Wang W-X, Fisher NS, Luoma SN (1996) Kinetic determinations of trace element bioaccumulation in the mussel Mytilus edulis. Mar Ecol Prog Ser 140:91–113

    Article  CAS  Google Scholar 

  • Warnau M, Fowler SW, Teyssié J-L (1996) Biokinetics of selected heavy metals and radionuclides in two marine macrophytes: the seagrass Posidonia oceanica and the alga Caulerpa taxifolia. Mar Environ Res 41:343–362

    Article  CAS  Google Scholar 

  • Warren L, Tessier A, Hare L (1998) Modelling cadmium accumulation by benthic invertebrates in situ: the relative contribution of sediment and overlying water reservoirs to organism cadmium concentrations. Limnol Oceanogr 43:1442–1454

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Wise SS, Xie H, Fukuda T et al (2014) Hexavalent chromium is cytotoxic and genotoxic to hawksbill sea turtle cells. Toxicol Appl Pharmacol 279:113–118. doi:10.1016/j.taap.2014.06.008

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the International Atomic Energy Agency (IAEA). The support of French Ecosphère Continentale et Côtière—Programme National Environnement Côtier (EC2CO-PNEC) and the Institut de Recherche pour le Développement (IRD) is also acknowledged. The IAEA is grateful for the support provided to its Environment Laboratories by the Government of the Principality of Monaco. LH was beneficiary of a PhD grant (CIFRE, France) supported by the Goro Nickel Company, New Caledonia. MW is an Honorary Senior Research Associate of the National Fund for Scientific Research (NFSR, Belgium).

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  1. Laetitia Hédouin

    Present address: PSL Research University: EPHE-UPVD-CNRS, USR 3278 CRIOBE, Laboratoire d’Excellence «CORAIL», PSL Research University, BP 1013, 98729, Papetoai, Moorea, French Polynesia

Authors and Affiliations

  1. International Atomic Energy Agency—Environment Laboratories (IAEA-EL), 4a Quai Antoine Ier, MC-98000, Monaco, Principality of Monaco

    Laetitia Hédouin, Marc Metian, Jean-Louis Teyssié & Michel Warnau

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

    Laetitia Hédouin

  3. Mediterranean Institute of Oceanography (MIO), Aix-Marseille Université, CNRS/INSU, Université de Toulon, IRD, UM 110, 13288, Marseille, France

    Laetitia Hédouin & Renaud Fichez

  4. USR378 EPHE CNRS UPVD—CRIOBE, Laboratoire d’Excellence CORAIL, BP1013, 98729, Papetoai, Moorea, French Polynesia

    Laetitia Hédouin

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  1. Laetitia Hédouin
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  2. Marc Metian
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Correspondence to Laetitia Hédouin.

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Hédouin, L., Metian, M., Teyssié, JL. et al. High contribution of the particulate uptake pathway to metal bioaccumulation in the tropical marine clam Gafrarium pectinatum . Environ Sci Pollut Res 25, 11206–11218 (2018). https://doi.org/10.1007/s11356-017-8562-z

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