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Delineating the role of calcium in shell formation and elemental composition of Corbicula fluminea (Bivalvia)

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Abstract

Calcium is one of the major constituents of bivalve shells. Other element impurities potentially record physical and chemical changes of the ambient environment during growth. It is commonly assumed that Ca2+ and other divalent ions may share the same transport mechanisms because of similar ionic radii and electrochemical properties. However, little effort has been devoted to bolstering this hypothesis. Here, we investigated the effects of Ca2+ on shell formation and element composition of the freshwater bivalve, Corbicula fluminea. Our results showed that increasing aqueous Ca2+ levels from 3 to 6 mM did not facilitate shell production. However, the amounts of Mn, Cu, and Pb incorporated into the shells significantly decreased, indicating the potential competition with Ca2+ in the same transport pathways. Furthermore, blocking the Ca2+ channels by lanthanum and Verapamil significantly reduced Mn, Cu, Zn, and Pb incorporation into the shells, and Mn/Cashell and Cu/Cashell decreased simultaneously when inhibiting the Ca2+-ATPase by ruthenium red. However, the amounts of Mg, Sr, and Ba incorporated into the shells were virtually unaffected, implying that intracellular Ca2+ transport mechanisms are not responsible for their incorporation into the shells. These findings help decipher underlying mechanisms responsible for the element partitioning between the ambient water and the shells.

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References

  • Allison, J. D., D. S. Brown & J. Kevin, 1991. MINTEQA2/PRODEFA2, a geochemical assessment model for environmental systems: version 3.0 user’s manual. Athens, GA: Environmental Research Laboratory, Office of Research and Development, U.S. Environmental Protection Agency.

  • Bellotto, V. R. & N. Miekeley, 2007. Trace metals in mussel shells and corresponding soft tissue samples: a validation experiment for the use of Perna perna shells in pollution monitoring. Analytical and Bioanalytical Chemistry 389: 769–776.

    Article  CAS  PubMed  Google Scholar 

  • Black, B. A., D. C. Gillespie, S. E. MacLellan & C. M. Hand, 2008. Establishing highly accurate production-age data using the tree-ring technique of crossdating: a case study for Pacific geoduck (Panopea abrupta). Canadian Journal of Fisheries and Aquatic Sciences 65: 2572–2578.

    Article  Google Scholar 

  • Bolotov, I. N., O. S. Pokrovsky, Y. Auda, J. V. Bespalaya, I. V. Vikhrev, M. Y. Gofarov, A. A. Lyubas, J. Viers & C. Zouiten, 2015. Trace element composition of freshwater pearl mussels Margaritifera spp. across Eurasia: testing the effect of species and geographic location. Chemical Geology 402: 125–139.

    Article  CAS  Google Scholar 

  • Bourgoin, B. P., 1990. Mytilus edulis shell as a bioindicator of lead pollution: considerations on bioavailability and variability. Marine Ecology Progress Series 61: 253–262.

    Article  CAS  Google Scholar 

  • Bruland, K. W., 1983. Trace elements in seawater. In Wong, C. S., K. W. Bruland, D. Burton & E. D. Goldberg (eds), Chemical oceanography. Academic Press, London: 157–220.

    Chapter  Google Scholar 

  • Campbell, P. G., 1995. Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model. In Tessier, A. & D. R. Turner (eds), Metal Speciation and Bioavailability in Aquatic Systems. Wiley, New York: 45–102.

    Google Scholar 

  • Carré, M., I. Bentaleb, O. Bruguier, E. Ordinola, N. T. Barrett & M. Fontugne, 2006. Calcification rate influence on trace element concentrations in aragonitic bivalve shells: evidences and mechanisms. Geochimica et Cosmochimica Acta 70: 4906–4920.

    Article  Google Scholar 

  • Carriker, M. R., R. E. Palmer, L. V. Sick & C. C. Jonhson, 1980. Interaction of mineral elements in sea water and shell of oysters (Crassostrea virginica (Gmelin)) cultured in controlled and natural systems. Journal of Experimental Marine Biology and Ecology 46: 279–296.

    Article  CAS  Google Scholar 

  • Coimbra, A. M., K. G. Ferreira, P. L. Fernandes & H. G. Ferreira, 1993. Calcium exchanges in Anodonta cygnea: barriers and driving gradients. Journal of Comparative Physiology 163: 196–202.

    CAS  Google Scholar 

  • Coimbra, J., J. Machado, P. L. Fernandes, H. G. Ferreira & K. G. Ferreira, 1988. Electrophysiology of the mantle of Anodonta cygnea. Journal of Experimental Biology 140: 65–88.

    Google Scholar 

  • Crenshaw, M. A., 1972. Inorganic composition of molluscan extrapallial fluid. Biological Bulletin 143: 506–512.

    Article  CAS  Google Scholar 

  • Deaton, L. E., 1981. Ion regulation in freshwater and brackish water bivalve mollusks. Physiological Zoology 54: 109–121.

    Article  CAS  Google Scholar 

  • Dietz, T. H., 1979. Uptake of sodium and chloride by freshwater mussels. Canadian Journal of Zoology 57: 156–160.

    Article  CAS  Google Scholar 

  • Fan, W., C. Li, S. Li, Q. Feng, L. Xie & R. Zhang, 2007. Cloning, characterization, and expression patterns of three sarco/endoplasmic reticulum Ca2+-ATPase isoforms from pearl oyster (Pinctada fucata). Acta Biochimica et Biophysica Sinica 39: 722–730.

    Article  CAS  PubMed  Google Scholar 

  • Gillikin, D. P., A. Lorrain, J. Navez, J. W. Taylor, L. André, E. Keppens, W. Baeyens & F. Dehairs, 2005. Strong biological controls on Sr/Ca ratios in aragonitic marine bivalve shells. Geochemistry Geophysics Geosystems 6: Q05009.

    Article  Google Scholar 

  • Gosling, E., 2003. An introduction to bivalves. Biology, Ecology and Culture. Fishing News Books, Blackwell, Oxford, Bivalve Molluscs.

    Book  Google Scholar 

  • Guerrero, J. & S. S. Martin, 1984. Verapamil, full spectrum Ca channel blocking agent: an overview. Medicinal Research Reviews 4: 87–109.

    Article  CAS  PubMed  Google Scholar 

  • Hatch, M. B., S. A. Schellenberg & M. L. Carter, 2013. Ba/Ca variations in the modern intertidal bean clam Donax gouldii: an upwelling proxy? Palaeogeography Palaeoclimatology Palaeoecology 373: 98–107.

    Article  Google Scholar 

  • Hincks, S. S. & G. L. Mackie, 1997. Effects of pH, calcium, alkalinity, hardness, and chlorophyll on the survival, growth, and reproductive success of zebra mussel (Dreissena polymorpha) in Ontario lakes. Canadian Journal of Fisheries and Aquatic Sciences 54: 2049–2057.

    Article  CAS  Google Scholar 

  • Jeffree, R. A., S. J. Markich, F. Lefebvre, M. Thellier & C. Ripoll, 1995. Shell microlaminations of the freshwater bivalve Hyridella depressa as an archival monitor of manganese water concentration: experimental investigation by depth profiling using secondary ion mass spectrometry (SIMS). Experientia 51: 838–848.

    Article  CAS  Google Scholar 

  • Kaehler, S. & C. D. McQuaid, 1999. Use of the fluorochrome calcein as an in situ growth marker in the brown mussel Perna perna. Marine Biology 133: 455–460.

    Article  Google Scholar 

  • Kastner, M., 1999. Oceanic minerals: their origin, nature of their environment and significance. Proceedings of the National Academy of Sciences 96: 3380–3387.

    Article  CAS  Google Scholar 

  • Klein, R. T., K. C. Lohman & C. W. Thayer, 1996. Sr/Ca and 13C/12C ratios in skeletal calcite of Mytilus trossulus: covariation with metabolic rate, salinity and carbon isotopic composition of sea water. Geochimica et Cosmochimica Acta 60: 4207–4221.

    Article  CAS  Google Scholar 

  • Kleypas, J. & C. Langdon, 2000. Overview of CO2-induced changes in seawater chemistry. Proceedings of the 9th International Coral Reef Symposium, Bali, Indonesia, 23–27 October 2000, 2: 1085–1089.

  • Krause-Nehring, J., T. Brey & S. R. Thorrold, 2012. Centennial records of lead contamination in northern Atlantic bivalves (Arctica islandica). Marine Pollution Bulletin 64: 233–240.

    Article  CAS  PubMed  Google Scholar 

  • Lucas, A. P. & G. Beninger, 1985. The use of physiological condition index in marine bivalve aquaculture. Aquaculture 44: 187–200.

    Article  Google Scholar 

  • Marin, F., N. L. Le Roy & B. Marie, 2012. The formation and mineralization of mollusk shells. Frontiers in Bioscience 4: 1099–1125.

    Article  Google Scholar 

  • Markich, S. J. & R. A. Jeffree, 1994. Absorption of divalent trace metals as analogues of calcium by Australian freshwater bivalves: an explanation of how water hardness reduces metal toxicity. Aquatic Toxicology 29: 257–290.

    Article  CAS  Google Scholar 

  • McConnaughey, T. A. & D. P. Gillikin, 2008. Carbon isotopes in mollusk shell carbonates. Geo-Marine Letters 28: 287–299.

    Article  CAS  Google Scholar 

  • McMahon, R. F., 1983. Ecology of an invasive pest bivalve, Corbicula. Mollusca 6: 505–561.

    Google Scholar 

  • McMahon, R. F., 2002. Evolutionary and physiological adaptations of aquatic invasive animals: r selection versus resistance. Canadian Journal of Fisheries and Aquatic Sciences 59: 1235–1244.

    Article  Google Scholar 

  • Mellina, E. & J. B. Rasmussen, 1994. Patterns in the distribution and abundance of zebra mussel (Dreissena polymorpha) in rivers and lakes in relation to substrate and other physicochemical factors. Canadian Journal of Fisheries and Aquatic Sciences 51: 1024–1036.

    Article  Google Scholar 

  • Millero, F. J., R. Feistel, D. G. Wright & T. J. McDougall, 2008. The composition of standard seawater and the definition of the reference-composition salinity scale. Deep-Sea Research 55: 50–72.

    Article  Google Scholar 

  • Murphy, W. A. & T. H. Dietz, 1976. The effects of salt depletion on blood and tissue ion concentrations in the freshwater mussel, Ligumia subrostrata (Say). Journal of Comparative Physiology 108: 233–242.

    Article  CAS  Google Scholar 

  • Nduku, W. K. & A. D. Harrison, 1976. Calcium as a limiting factor in the biology of Biomphalaria pfeifferi (Krauss) (Gastropoda: Planorbidae). Hydrobiologia 49: 143–170.

    Article  CAS  Google Scholar 

  • Phillips, D. J. H., 1976. The common mussel Mytilus edulis as an indicator of pollution by zinc, lead, and copper, I: effects on environmental variables on uptake of metals. Marine Biology 38: 59–69.

    Article  CAS  Google Scholar 

  • Prezant, R. S. & A. Tan-Tiu, 1985. Comparative shell microstructure of North American Corbicula (Bivalvia: Sphaeriacea). Veliger 27: 312–319.

    Google Scholar 

  • Qiu, J. W. & W. X. Wang, 2005. Effects of calcium on the uptake and elimination of cadmium and zinc in Asiatic clams. Archives of Environmental Contamination and Toxicology 48: 278–287.

    Article  CAS  PubMed  Google Scholar 

  • Richardson, C. A., S. R. N. Chenery & J. M. Cook, 2001. Assessing the history of trace metal (Cu, Zn, Pb) contamination in the North Sea through laser ablation ICP-MS of horse mussel Modiolus modiolus shells. Marine Ecology Progress Series 211: 157–167.

    Article  CAS  Google Scholar 

  • Schöne, B. R., 2013. Arctica islandica (Bivalvia): a unique paleoenvironmental archive of the northern North Atlantic Ocean. Global and Planetary Change 111: 199–225.

    Article  Google Scholar 

  • Schöne, B. R., Z. Zhang, D. Jacob, D. P. Gillikin, T. Tütken, D. Garbe-Schönberg & A. Soldati, 2010. Effect of organic matrices on the determination of the trace element chemistry (Mg, Sr, Mg/Ca, Sr/Ca) of aragonitic bivalve shells (Arctica islandica) – comparison of ICP-OES and LA-ICP-MS data. Geochemical Journal 44: 23–37.

    Article  Google Scholar 

  • Schöne, B. R., Z. Zhang, P. Radermacher, J. Thébault, D. E. Jacob, E. V. Nunn & A. F. Maurer, 2011. Sr/Ca and Mg/Ca ratios of ontogenetically old, long-lived bivalve shells (Arctica islandica) and their function as paleotemperature proxies. Palaeogeography Palaeoclimatology Palaeoecology 302: 52–64.

    Article  Google Scholar 

  • Shannon, R. D., 1976. Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Crystallographica B 32: 751–767.

    Google Scholar 

  • Shirai, K., B. R. Schöne, T. Miyaji, P. Radermacher, R. A. Krause Jr. & K. Tanabe, 2014. Assessment of the mechanism of elemental incorporation into bivalve shells (Arctica islandica) based on elemental distribution at the microstructural scale. Geochimica et Cosmochimica Acta 126: 307–320.

    Article  CAS  Google Scholar 

  • Shi, D. L. & W. X. Wang, 2004. Understanding the differences in Cd and Zn bioaccumulation and subcellular storage among different populations of marine clams. Environmental Science & Technology 38: 449–456.

    Article  CAS  Google Scholar 

  • Simkiss, K. & M. G. Taylor, 1989. Metal fluxes across the membranes of aquatic organisms. Aquatic Sciences 1: 173–188.

    CAS  Google Scholar 

  • Sprung, M., 1987. Ecological requirements of developing Dreissena polymorpha eggs. Archiv für Hydrobiologie, Supplementband 79: 69–86.

    Google Scholar 

  • Takesue, R. K., C. R. Bacon & J. K. Thompson, 2008. Influences of organic matter and calcification rate on trace elements in aragonitic estuarine bivalve shells. Geochimica et Cosmochimica Acta 72: 5431–5445.

    Article  CAS  Google Scholar 

  • Thébault, J., L. Chauvaud, J. Clavier, R. Fichez & E. Morize, 2006. Evidence of a 2-day periodicity of striae formation in the tropical scallop Comptopallium radula using calcein marking. Marine Biology 149: 257–267.

    Article  Google Scholar 

  • Thébault, J., L. Chauvaud, S. L. Helguen, J. Clavier, A. Barats, S. Jacquet, C. Pécheyran & D. Amouroux, 2009. Barium and molybdenum records in bivalve shells: geochemical proxies for phytoplankton dynamics in coastal environments? Limnology and Oceanography 54: 1002–1014.

    Article  Google Scholar 

  • Viarengo, A. & J. A. Nott, 1993. Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comparative Biochemistry and Physiology C 104: 355–372.

    Article  Google Scholar 

  • Verbost, P. M., J. Van Rooij, G. Flik, R. A. C. Lock & S. E. Wendelaar Bonga, 1989. The movement of cadmium through freshwater trout branchial epithelium and its interference with Ca transport. Journal of Experimental Biology 145: 185–197.

    CAS  Google Scholar 

  • Vinogradov, G. A., N. F. Smirnova, V. A. Sokalov & A. A. Bruznitsky, 1993. Influence of chemical composition of the water on the mollusk Dreisenna polymorpha. In Nalepa, T. F. & D. W. Schloesser (eds), Zebra Mussels: Biology, Impacts, and Control. Lewis Publishers/CRC Press, Boca Raton: 283–293.

    Google Scholar 

  • Wada, K. & T. Fujinuki, 1976. Biomineralization in bivalve molluscs with emphasis on the chemical composition of the extrapallial fluid. In Bryan, N. M. & K. M. Wilbur (eds), Mechanisms of Mineralization in the Invertebrates and Plants. University of South Carolina Press, Georgetown: 175–190.

    Google Scholar 

  • Wanamaker Jr., A. D., K. J. Kreutz, B. R. Schöne, K. A. Maasch, A. Pershing, H. W. Borns, D. S. Introne & S. Feindel, 2009. A late Holocene paleo-productivity record in the Western Gulf of Maine, USA, inferred from growth histories of the long-lived ocean quahog (Arctica islandica). International Journal of Earth Sciences 98: 19–29.

    Article  CAS  Google Scholar 

  • Watson, E. L., F. F. Vincenzi & P. W. Davis, 1971. Ca2+-activated membrane ATPase: selective inhibition by ruthenium red. Biochimica et Biophysica Acta 249: 606–610.

    Article  CAS  PubMed  Google Scholar 

  • Wheeler, A. P., 1992. Mechanisms of molluscan shell formation. In Bonucci, E. (ed.), Calcification in biological systems. CRC Press, Boca Raton, FL: 179–216.

    Google Scholar 

  • Wilbur, K. M. & A. S. M. Saleuddin, 1983. Shell formation. In Saleuddin, A. S. M. & K. M. Wilbur (eds), The Mollusca 4. Physiology. Academic Press, New York.

    Google Scholar 

  • Zhao, L. Q., B. R. Schöne & R. Mertz-Kraus, 2015. Controls on strontium and barium incorporation into freshwater bivalve shells (Corbicula fluminea). Palaeogeography Palaeoclimatology Palaeoecology. doi:10.1016/j.palaeo.2015.11.040.

    Google Scholar 

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Acknowledgments

We thank Michael Maus (Institute of Geosciences, University of Mainz) for his assistance in measuring the concentrations of elements of water samples. We also thank two anonymous reviewers for their comments which helped to improve the manuscript. This study has been made possible by a research grant within the framework (FP7) of the Marie Curie International Training Network ARAMACC (European Union's Seventh Framework Programme FP7/2007–2013/ under REA grant agreement number 604802) to BRS and by the DFG (SCHO793/13) to BRS.

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  1. Institute of Geosciences, University of Mainz, Joh.-J.-Becher-Weg 21, 55128, Mainz, Germany

    Liqiang Zhao, Bernd R. Schöne & Regina Mertz-Kraus

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  1. Liqiang Zhao
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Correspondence to Bernd R. Schöne.

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Zhao, L., Schöne, B.R. & Mertz-Kraus, R. Delineating the role of calcium in shell formation and elemental composition of Corbicula fluminea (Bivalvia). Hydrobiologia 790, 259–272 (2017). https://doi.org/10.1007/s10750-016-3037-7

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