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Comparison of trace metal bioavailabilities in European coastal waters using mussels from Mytilus edulis complex as biomonitors

Abstract

Mussels from Mytilus edulis complex were used as biomonitors of the trace metals Fe, Mn, Pb, Zn, and Cu at 17 sampling sites to assess the relative bioavailability of metals in coastal waters around the European continent. Because accumulated metal concentrations in a given area can differ temporally, data were corrected for the effect of season before large-scale spatial comparisons were made. The highest concentration of Fe was noted in the North Sea and of Mn in the Baltic. Increased tissue concentrations of Pb were recorded in the mussels from the Bay of Biscay and the Baltic Sea. Low concentrations of metals were determined in the mussels from the Mediterranean Sea and the Northern Baltic. Relatively low geographic variations of Cu and Zn indicate that mussels are able to partially regulate accumulated body concentrations, which means Cu and Zn are, to some extent, independent of environmental concentrations.

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References

  • Amiard, J. C., Amiard-Trinquet, C., Berthet, B., & Métayer, C. (1986). Contribution to the ecotoxicological study of cadmium, lead, copper and zinc in the mussel Mytilus edulis. Marine Biology (Berlin), 90, 425–431. doi:10.1007/BF00428566.

    Article  CAS  Google Scholar 

  • Andral, B., Stanisiére, J. Y., Sauzade, D., Damier, E., Thebault, H., Galgani, F., et al. (2004). Monitoring chemical contamination levels in the Mediterranean based on the use of mussel caging. Marine Pollution Bulletin, 49, 704–712. doi:10.1016/j.marpolbul.2004.05.008.

    Article  CAS  Google Scholar 

  • Angulo, E. (1996). The Tomlinson pollution load index applied to heavy metal, ‘Mussel-Watch’ data: A useful index to assess coastal pollution. The Science of the Total Environment, 187, 19–56. doi:10.1016/0048–9697(96)05128–5.

    Article  CAS  Google Scholar 

  • Baeyens, W. (1998). Evolution of trace metal concentrations in the Sheldt estuary (1978–1995). A comparison with estuarine and ocean levels. Hydrobiologia, 366, 157–167. doi:10.1023/A:1003136613574.

    Article  Google Scholar 

  • BIOCOMBE. (2006). Final periodic report and seventh management report November 2002–April 2006, The impact of biodiversity changes in coastal marine benthic ecosystems (pp. 270) Yerseke.

  • Birkun, A., Jr. (2002). Cetacean habitat loss and degradation in the Black Sea. In G. Notarbartolo di Sciara (Ed.), Cetaceans of the Mediterranean and Black Seas: State of knowledge and conservation strategies. Raport ACCOBAMS Secretariat, (pp. 2–19) Monaco 8, Section 8.

  • Blackmore, G., & Wang, W. X. (2003). Comparison of metal accumulation in mussels at different local and global scales. Environmental Toxicology and Chemistry, 22(2), 388–395. doi:10.1897/1551–5028(2003)022<0388:COMAIM>2.0.CO;2.

    Article  CAS  Google Scholar 

  • Borchardt, T., Burchert, S., Hablizel, L., Karbe, L., & Zeitner, R. (1988). Trace metal concentrations in mussels: Comparison between estuarine, coastal and offshore regions in the southeastern North Sea from 1983 to 1986. Marine Ecology Progress Series, 42, 17–31. doi:10.3354/meps042017.

    Article  CAS  Google Scholar 

  • Boyden, C. R. (1974). Trace element content and body size in molluscs. Nature, 251, 311–314. doi:10.1038/251311a0.

    Article  CAS  Google Scholar 

  • Cantillo, A. Y. (1998). Comparison of results of mussel watch programs of the United States and France with worldwide mussel watch studies. Marine Pollution Bulletin, 36, 712–717. doi:10.1016/S0025-326X(98)00049-6.

    Article  CAS  Google Scholar 

  • Casas, S., Cossa, D., Gonzalez, J. L., Bacher, C., & Andral, B. (2004). Modeling trace metal accumulation in the Mediterranean mussel, Mylilus galloprovincialis. Rapport du Congrès de la Commission Internationale pour l’Exploration Scientifique de la Mer Méditerranée, 37, 306–308.

    Google Scholar 

  • Conti, M. E., & Cecchetti, G. (2003). A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environmental Research, 93, 99–112. doi:10.1016/S0013–9351(03)00012–4.

    Article  CAS  Google Scholar 

  • Conti, M. E., Tudino, M. B., Muse, J. O., & Cecchetti, G. (2002). Biomonitoring of heavy metals and their species in the marine environment: The contribution of atomic absorption spectroscopy and inductively coupled plasma spectroscopy. Research Trends in Applied Spectroscopy, 4, 295–324.

    CAS  Google Scholar 

  • Falandysz, J., Trzosiñska, A., Szefer, P., Warzocha, J., & Draganik, B. (2000). The Baltic Sea, especially southern and eastern regions. In C. Scheppard (Ed.), Seas at the millennium (pp. 91–112). Amsterdam: Elsevier.

    Google Scholar 

  • Gerringa, L. J. A., Poortvliet, T. C. W., & Hummel, H. (1996). Comparison of chemical speciation of copper in the oosterschelde and westerschelde estuaries, The Netherlands. Estuarine, Coastal and Shelf Science, 42, 629–643. doi:10.1006/ecss.1996.0041.

    Article  CAS  Google Scholar 

  • Gosling, E. M. (1992). Systematics and geographic distribution of Mytilus. In: E. M. Gosling (Ed.), The mussel Mytilus: ecology, physiology, genetics and culture (pp. 1–20). Amsterdam: Elsevier.

    Google Scholar 

  • Green, N., Bjeerkeng, B., Hylland, K., Ruus, A., & Rygg, B. (2003). Hazardous substances in the European marine environment: Trends in metals and persistent organic pollutants (pp. 6–60). Copenhagen: European Environment Agency.

    Google Scholar 

  • HELCOM (2006). Hazardous substances in the Baltic Sea (pp. 2–17). Finland: HELCOM.

    Google Scholar 

  • Helios Rybicka, E. (1996). Impact of mining and metallurgical industries on the environment in Poland. Applied Geochemistry, 11, 3–9. doi:10.1016/0883-2927(95)00083-6.

    Article  Google Scholar 

  • Hellou, J., & Law, R. J. (2003). Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health. Environmental Pollution, 126, 407–416. doi:10.1016/S0269-7491(03)00231-8.

    Article  CAS  Google Scholar 

  • Hummel, H., Modderman, R., Amiard-Triquet, C., Rainglet, F., van Duijn, Y., Herssevoort, M., et al. (1997). A comparative study on the relation between copper and condition in marine bivalves and the relation with copper in the sediment. Aquatic Toxicology (Amsterdam, Netherlands), 38, 165–181. doi:10.1016/S0166-445X(96)00832-6.

    CAS  Google Scholar 

  • Hummel, H., Colucci, F., Bogaards, R. H., & Strelkov, P. (2001). Genetic traits in the bivalve Mytilus from Europe, with an emphasis on Arctic populations. Polar Biology, 24, 44–52. doi:10.1007/s003000000174.

    Article  Google Scholar 

  • Lobel, P. B., & Wright, D. A. (1982). Relationship between body zinc concentration and allometric growth measurements in the mussel Mytilus edulis. Marine Biology (Berlin), 66, 145–150. doi:10.1007/BF00397187.

    Article  CAS  Google Scholar 

  • Lobel, P. B., Belkhode, S. P., Jackson, S. E., & Longerich, H. P. (1990). Recent taxonomic discoveries concerning the mussels Mytilus implications for biomonitoring. Archives of Environmental Contamination and Toxicology, 19, 508–512. doi:10.1007/BF01059068.

    Article  CAS  Google Scholar 

  • Lobel, P. B., Bajdik, C. D., Belkhode, S. P., Jackson, S. E., & Longerich, H. P. (1991). Improved protocol for collecting mussel watch specimens taking into account sex, condition, shell shape, and chronological age. Archives of Environmental Contamination and Toxicology, 21, 409–414. doi:10.1007/BF01060364.

    Article  Google Scholar 

  • Millward, G. E., Morris, A. W., & Tappin, A. D. (1998). Trace metals at two sites in the southern North Sea: Results from a sediment resuspension study. Continental Shelf Research, 18, 1381–1400. doi:10.1016/S0278-4343(98)00049-1.

    Article  Google Scholar 

  • Miramand, P., Guyot, T., Rybarczyk, H., Elkaïm, B., Mounny, P., Dauvin, J. C., et al. (2001). Contamination of the biological compartment in the Seine estuary by Cd, Cu, Pb and Zn. Estuaries, 24(6B), 1056–1065. doi:10.2307/1353017.

    Article  CAS  Google Scholar 

  • Morrisey, D. J., Underwood, A. J., Stark, J. S., & Howitt, L. (1994). Temporal variation in concentrations of heavy metals in marine sediments. Estuarine, Coastal and Shelf Science, 38, 271–282. doi:10.1006/ecss.1994.1018.

    Article  CAS  Google Scholar 

  • Mubiana, V. K., Qadah, D., Meys, J., & Blust, R. (2005). Temporal and spatial trends in heavy metal concentrations in the marine mussel Mytilus edulis from the Western Scheldt estuary (The Netherlands). Hydrobiologia, 540, 169–180. doi:10.1007/s10750-004-7134-7.

    Article  CAS  Google Scholar 

  • O’Leary, C., & Breen, J. (1998). Seasonal variation of heavy metals in Mytilus edulis, Fucus vesiculosus and sediment from the Shannon Estuary. Proceedings of the Royal Irish Academy. Section B: Biological, Geological, and Chemical Science, 98b(3), 153–169.

    Google Scholar 

  • Phillips, D. J. H., & Rainbow, P. S. (1988). Barnacles and mussels as biomonitors of trace elements: A comparative study. Marine Ecology Progress Series, 49, 83–93. doi:10.3354/meps049083.

    Article  CAS  Google Scholar 

  • Presa, P., Pérez, M., & Diz, A. P. (2002). Polymorphic microsatellite markers for blue mussels (Mytilus spp.). Conservation Genetics, 3, 441–443. doi:10.1023/A:1020571202907.

    Article  CAS  Google Scholar 

  • Radenac, G., Miramand, P., & Tardy, J. (1997). Search for impact of a dredged material disposal site on growth and metal contamination of Mytilus edulis (L.) in Charente-Maritime (France). Marine Pollution Bulletin, 34(9), 721–729. doi:10.1016/S0025-326X(97)00011-8.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (1995). Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin, 31, 183–192. doi:10.1016/0025-326X(95)00116-5.

    Article  CAS  Google Scholar 

  • Rainbow, P. S. (1999). Bioaccumulation of trace metals: Biological significance. Oceanis, 25(4), 547–561.

    CAS  Google Scholar 

  • Rainbow, P. S., Wolowicz, M., Fialkowski, W., Smith, B. D., & Sokolowski, A. (2000). Biomonitoring of trace metals in the Gulf of Gdansk, using mussels (Mytilus trossulus) and barnacles (Balanus improvisus). Water Research, 34(6), 1823–1829. doi:10.1016/S0043-1354(99)00345-0.

    Article  CAS  Google Scholar 

  • Rainbow, P. S., Fialkowski, W., Sokolowski, A., Smith, B. D., & Wolowicz, M. (2004). Geographical and seasonal variation of trace metal bioavailabilities in the Gulf of Gdansk, Baltic Sea using mussels (Mytilus trossulus) and barnacles (Balanus improvisus) as biomonitors. Marine Biology (Berlin), 144, 271–286. doi:10.1007/s00227-003-1197-2.

    Article  CAS  Google Scholar 

  • Regoli, F. (1998). Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean mussel Mytilus galloprovincialis. Archives of Environmental Contamination and Toxicology, 34, 48–63. doi:10.1007/s002449900285.

    Article  CAS  Google Scholar 

  • Regoli, F., Hummel, H., Amiard-Triquet, C., Larroux, C., Sukhotin, A., & Bertoli, E. (1998). Trace metals and variations of antioxidant enzymes in Arctic bivalve populations. Archives of Environmental Contamination and Toxicology, 35(4), 594–601. doi:10.1007/s002449900421.

    Article  CAS  Google Scholar 

  • Riget, F., Johansen, P., & Asmund, G. (1996). Influence of length on element concentrations in blue mussels (Mytilus edulis). Marine Pollution Bulletin, 32(10), 745–751. doi:10.1016/0025-326X(96)00067-7.

    Article  CAS  Google Scholar 

  • Saavedra, Y., González, A., Fernández, P., & Blanco, J. (2004). The effect of size on trace metal in raft cultivated mussels (Mytilus galloprovincialis). The Science of the Total Environment, 318, 115–124. doi:10.1016/S0048-9697(03)00402-9.

    Article  CAS  Google Scholar 

  • Seed, R. (1992). Systematics evolution and distribution of mussel belonging to the genus Mytilus. American Malacological Bulletin, 9, 123–137.

    Google Scholar 

  • Sokal, R. R., & Rohlf, F. J. (1995). Biometry (pp. 887). New York: Freeman.

    Google Scholar 

  • Sokolowski, A., Bawazir, A. S., & Wolowicz, M. (2004). The effect of seasonal cycle, weight and sex of individuals on trace metal concentrations in the brown mussel Perna perna from the coastal waters off Yemen (Gulf of Aden). Archives of Environmental Contamination and Toxicology, 46, 67–80. doi:10.1007/s00244-003-2164-0.

    Article  CAS  Google Scholar 

  • Soto, M., Kortabitarte, M., & Marigòmez, I. (1995). Bioavailable heavy metals in estuarine waters as assessed by metal/shell-weight indices in sentinel mussels Mytilus galloprovincialis. Marine Ecology Progress Series, 125, 127–136. doi:10.3354/meps125127.

    Article  CAS  Google Scholar 

  • Storelli, M. M., Storelli, A., & Marcotrigiano, G. O. (2000). Heavy metals in mussels (Mytilus galloprovincialis) from the Ionian Sea, Italy. Journal of Food Protection, 63(2), 273–276.

    CAS  Google Scholar 

  • Szefer, P. (2002). Metals, metalloids and radionuclides in the Baltic sea ecosystem (752 pp.). Amsterdam: Elsevier.

    Google Scholar 

  • Szefer, P., Glasby, G. P., Pempkowiak, J., & Kaliszan, R. (1995). Extraction studies of heavy-metal pollutants in surficial sediments from the southern Baltic Sea off Poland. Chemical Geology, 120, 111–126. doi:10.1016/0009-2541(94)00103-F.

    Article  CAS  Google Scholar 

  • Szefer, P., Frelek, K., Szefer, K., Lee, C. B., Kim, B. S., Warzocha, J., et al. (2002). Distribution and relationships of trace metals in soft tissue, byssus and shells of Mytilus edulis trossulus from the southern Baltic. Environmental Pollution, 120, 423–444. doi:10.1016/S0269-7491(02)00111-2.

    Article  CAS  Google Scholar 

  • Szefer, P., Fowler, S. W., Ikuta, K., Paez Osuna, F., Ali, A. A., Kim, B. S., et al. (2006). A comparative assessment of heavy metal accumulation in soft parts and byssus of mussels from subarctic, temperate, subtropical and tropical marine environments. Environmental Pollution, 139, 70–78. doi:10.1016/j.envpol.2005.04.031.

    Article  CAS  Google Scholar 

  • Walker, C. H., Hopkin, S. P., Sibly, R. M., & Peakall, D. B. (2001). Principles of ecotoxicology. London: Taylor & Francis.

    Google Scholar 

  • Wallace, W. G., Lee, B. G., & Luoma, S. N. (2003). Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM). Marine Ecology Progress Series, 249, 183–197. doi:10.3354/meps249183.

    Article  CAS  Google Scholar 

  • Yngvadóttir, E., Halldórsdóttir, H., Ragnarsdóttir, T., & Arnadóttir, E. (2002). Monitoring of the marine biosphere around Iceland in 1998–2000 (pp. 2–80). Reykjavik: The AMSUM group.

    Google Scholar 

  • Zatsepin, V. I., Filatova, Z. A., & Shilejko, A. A. (1988). Klass dwustworchatyie molljuski (Bivalvia). In R. K. Pasternak (Ed.), Zhizn’Zhivotnyh-Molljuski-Igłokożie-Chlenistonogie (The life of animals-molluscs) (pp. 65–112). Moscow: Prosveshchenie, Izdatelstvo, (in Russian).

    Google Scholar 

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Correspondence to Joanna Ewa Przytarska.

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Przytarska, J.E., Sokołowski, A., Wołowicz, M. et al. Comparison of trace metal bioavailabilities in European coastal waters using mussels from Mytilus edulis complex as biomonitors. Environ Monit Assess 166, 461–476 (2010). https://doi.org/10.1007/s10661-009-1015-5

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  • DOI: https://doi.org/10.1007/s10661-009-1015-5

Keywords

  • Mytilus
  • Trace metals
  • European marginal seas
  • Biomonitoring
  • Pollution
  • Seasonal variation coefficient