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Complexity of spatial and temporal trends in metal concentrations in macroinvertebrate biomonitor species in the Severn Estuary and Bristol Channel

Published online by Cambridge University Press:  14 January 2011

David J. Bird ,
Sabine Duquesne ,
Steeg D. Hoeksema ,
William J. Langston  and
Ian C. Potter
David J. Bird*
Affiliation:
Department of Life Sciences, University of the West of England, Coldharbour Lane, Bristol, BS16 1QY, UK
Sabine Duquesne
Affiliation:
Department of System Ecotoxicology, Helmholtz Centre for Environmental Research, UFZ Permoserstrasse 15, D-04318 Leipzig, Germany
Steeg D. Hoeksema
Affiliation:
Centre for Fish and Fisheries Research, School of Biology and Biotechnology, Murdoch University, South Street, Murdoch, 6150, WesternAustralia
William J. Langston
Affiliation:
Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB, UK
Ian C. Potter
Affiliation:
Centre for Fish and Fisheries Research, School of Biology and Biotechnology, Murdoch University, South Street, Murdoch, 6150, WesternAustralia
*
Correspondence should be addressed to: D.J. Bird, Department of Life Sciences, University of the West of England, Coldharbour Lane, Bristol, BS16 1QY, UK email: david.bird@uwe.ac.uk
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Abstract

Cadmium, chromium, copper, nickel, lead and zinc concentrations in the bivalve mollusc Macoma balthica and the polychaete annelids Hediste diversicolor and Arenicola marina were measured, during winter and summer, at sites throughout the Severn Estuary and Bristol Channel. The mean concentration of each metal in A. marina was greater in the lower Severn Estuary than in the far less contaminated outer Bristol Channel and the concentration of a given metal, e.g. Cr, in a species occasionally peaked at a site, reflecting local metal contamination. The concentrations of each metal in each of these biomonitor species almost invariably differed significantly among sites and often seasons and there were sometimes interactions between site and season. This indicates that the various factors that determine the concentration of a metal in a species operate in a complex manner and that their individual effects can vary among sites and/or seasons. The rank order of each metal concentration in each species at a site within the estuary frequently did not match the sequence for the concentration of that metal measured in the sediment at that site at the same time. This lack of correspondence is likely to be due, at least in part, to one or both of the following: (1) variations in the bioavailability of certain metals among sites due to differences in such features as the metal-binding properties of the sediments; (2) the effects of the constant transport and redistribution of the sediments and thus also of their associated trace metals by the very strong tidal action that characterizes the Severn Estuary. This would mean that single time measurements do not accurately reflect the overall trace metal environment to which the biomonitor organism had been exposed in the weeks/months prior to sampling. Marked differences in the concentrations of certain metals, e.g. Cu and Zn, in co-occurring biomarker species could frequently be related to differences between the ability of these species to regulate certain metals. Non-metric multi-dimensional scaling ordination and associated tests emphasize that the relationships between the concentrations of the various metals differed markedly among species and between sites and seasons in individual species and elucidated which metals contributed most to those differences. If the proposed scheme for harnessing tidal power in the Severn Estuary proceeds, the data in this paper provide a baseline for assessing the impact of such major changes on the bioavailability of trace metals in this estuary. This information will also be invaluable for predicting the changes likely to occur in other estuaries that become subjected to major structural changes.

Keywords

trace metalsbenthic macroinvertebratesmacrotidal estuariesbiomonitoringsite and seasonal effectstidal power
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 1 , February 2011 , pp. 139 - 153
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Amiard, J.C., Amiard-Triquet, C., Berthet, B. and Metayer, C. (1987) Comparative-study of the patterns of bioaccumulation of essential (Cu, Zn) and nonessential (Cd, Pb) trace-metals in various estuarine and coastal organisms. Journal of Experimental Marine Biology and Ecology 106, 73–89.CrossRefGoogle Scholar
Amiard, J.C., Geffard, A., Amiard-Triquet, C. and Crouzet, C. (2007) Relationship between the lability of sediment-bound metals (Cd, Cu, Zn) and their bioaccumulation in benthic invertebrates. Estuarine, Coastal and Shelf Science 72, 511–521.CrossRefGoogle Scholar
Badsha, K.S. and Sainsbury, M. (1977) Uptake of zinc, lead and cadmium by young whiting in the Severn Estuary. Marine Pollution Bulletin 8, 164–166.CrossRefGoogle Scholar
Badsha, K.S. and Sainsbury, M. (1978) Some aspects of the biology and heavy metal accumulation of the fish Liparis liparus in the Severn Estuary. Estuarine, and Coastal Marine Science 7, 381–391.CrossRefGoogle Scholar
Bassindale, R. (1943) Studies on the biology of the Bristol Channel. XI. The physical environment and intertidal fauna of the southern shores of the Bristol Channel and Severn Estuary. Journal of Ecology 31, 1–29.CrossRefGoogle Scholar
Bird, D.J., Rotchell, J.M., Hesp, S.A., Newton, L.C., Hall, N.G. and Potter, I.C. (2008) To what extent are hepatic concentrations of heavy metals in Anguilla anguilla at a site in a contaminated estuary related to body size and age and reflected in the metallothionein concentrations? Environmental Pollution 151, 641–651.CrossRefGoogle Scholar
Boyden, C.R., Crothers, J.H., Little, C. and Mettam, C. (1977) The intertidal invertebrate fauna of the Severn Estuary. Field Studies 4, 477–554.Google Scholar
Bresler, V., Abelson, A., Feldstein, T., Mokady, O., Fishelson, L. and Rosenfeld, M. (2003) Marine molluscs in environmental monitoring. I. Cellular and molecular responses. Helgoland Marine Research 57, 157–165.CrossRefGoogle Scholar
Bryan, G.W. and Hummerstone, L.G. (1973) Adaptation of polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. Journal of the Marine Biological Association of the United Kingdom 53, 839–857.CrossRefGoogle Scholar
Bryan, G.W., Langston, W.J. and Hummerstone, L.G. (1980) The use of biological indicators of heavy metal contamination in estuaries. Marine Biological Association of the United Kingdom Occasional Publications, No. 1, 73 pp.Google Scholar
Butterworth, J., Lester, P. and Nickless, G. (1972) Distribution of heavy metals in the Severn Estuary. Marine Pollution Bulletin 3, 72–74.CrossRefGoogle Scholar
Claridge, P.N., Potter, I.C. and Hardisty, M.W. (1986) Seasonal changes in movements, abundance, size composition and diversity of the fish fauna of the Severn Estuary. Journal of the Marine Biological Association of the United Kingdom 66, 229–258.CrossRefGoogle Scholar
Clarke, K.R. (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. (2006) PRIMER v6: user manual/tutorial. Plymouth: PRIMER-E.Google Scholar
Culshaw, C., Newton, L.C., Weir, I. and Bird, D.J. (2002) Concentrations of Cd, Zn and Cu in sediments and brown shrimp (Crangon crangon L.) from the Severn Estuary and Bristol Channel, UK. Marine Environmental Research 54, 331–334.CrossRefGoogle Scholar
Depledge, M.H. and Rainbow, P.S. (1990) Models of regulation and accumulation of trace metals in marine invertebrates. Comparative Biochemistry and Physiology C—Pharmacology, Toxicology and Endocrinology 97, 1–7.Google Scholar
Duquesne, S., Newton, L.C., Giusti, L., Marriott, S.B., Stark, H.J. and Bird, D.J. (2006) Evidence for declining levels of heavy-metals in the Severn Estuary and Bristol Channel, UK and their spatial distribution in sediments. Environmental Pollution 143, 187–196.CrossRefGoogle ScholarPubMed
Duquesne, S. and Riddle, M.J. (2002) Biological monitoring of heavy-metal contamination in coastal waters off Casey Station, Windmill Islands, East Antarctica. Polar Biology 25, 206–215.CrossRefGoogle Scholar
Ellis, J.C. (2002) Water quality trends in the Severn Estuary. Bristol: Environment Agency, pp. 138.Google Scholar
Engel, D.W. and Fowler, B.A. (1979) Factors influencing cadmium accumulation and its toxicity to marine organisms. Environmental Health Perspectives 28, 81–88.CrossRefGoogle ScholarPubMed
Environment Agency (1997) Severn Estuary strategy joint issues report. Bristol: Environment Agency, pp. 173 .Google Scholar
Ferns, P.N. (1984) Birds of the Bristol Channel and Severn Estuary. Marine Pollution Bulletin 15, 76–81.CrossRefGoogle Scholar
Frangipane, G., Ghirardini, A.V., Collavini, F., Zaggia, L., Pesce, A. and Tagliapietra, D. (2005) Heavy metals in Hediste diversicolor (Polychaeta: Nereididae) and salt marsh sediments from the lagoon of Venice (Italy). Chemistry and Ecology 21, 441–454.CrossRefGoogle Scholar
Griscom, S.B., Fisher, N.S., Aller, R.C. and Lee, B.G. (2002) Effects of gut chemistry in marine bivalves on the assimilation of metals from ingested sediment particles. Journal of Marine Research 60, 101–120.CrossRefGoogle Scholar
Harper, D.J. (1991) The distribution of dissolved cadmium, lead and copper in the Bristol Channel and the outer Severn Estuary. Marine Chemistry 33, 131–143.CrossRefGoogle Scholar
Henderson, P.A. and Bird, D.J. (2010) Fish and macro-crustacean communities and their dynamics in the Severn Estuary. Marine Pollution Bulletin 61, 100–114.CrossRefGoogle ScholarPubMed
Jonas, P.J.C. and Millward, G.C. (2010) Metals and nutrients in the Severn Estuary and Bristol Channel: contemporary inputs and distributions. Marine Pollution Bulletin 61, 52–67.CrossRefGoogle ScholarPubMed
Langston, W.J., Bebianno, M.J. and Burt, G.R. (1998) Metal handling strategies in molluscs. In Langston, W.J. and Bebianno, M.J. (eds) Metal metabolism in aquatic environments. Dordrecht: Kluwer Academic Publishers, pp. 219–283.CrossRefGoogle Scholar
Langston, W.J., Chesman, B.S., Burt, G.R., Hawkins, S.J., Readman, J. and Worsfold, P. (2003) Characterization of the South West European Marine Sites: The Severn Estuary pSAC, SPA. Marine Biological Association of the United Kingdom Occasional Publications, No. 13, pp. 206.Google Scholar
Langston, W.J., Jonas, P.J.C. and Millward, G.E. (2010a) The Severn Estuary and Bristol Channel: a 25 year critical review. Marine Pollution Bulletin, 61, 1–4.CrossRefGoogle Scholar
Langston, W.J., Pope, N.D., Jonas, P.J.C., Nikitic, C., Field, M.D.R., Dowell, B., Shilloabeer, N., Swarbrick, R.H. and Brown, A.R. (2010b) Contaminants in fine sediments and their consequences for biota of the Severn Estuary. Marine Pollution Bulletin 61, 68–82.CrossRefGoogle ScholarPubMed
Luoma, S.N. and Rainbow, P.S. (2005) Why is metal bioaccumulation so variable? Biodynamics as a unifying concept. Environmental Science and Technology 39, 1921–1931.CrossRefGoogle ScholarPubMed
Martin, M.H., Nickless, G. and Stenner, R.D. (1997) Concentrations of cadmium, copper, lead, nickel and zinc in the alga Fucus serratus in the Severn Estuary from 1971 to 1995. Chemosphere 34, 325–334.CrossRefGoogle Scholar
Matozzo, V., Ballarin, L., Pampanin, D.M. and Marin, M.G. (2001) Effects of copper and cadmium exposure on functional responses of hemocytes in the clam, Tapes philippinarum. Archives of Environmental Contamination and Toxicology 41, 163–170.CrossRefGoogle ScholarPubMed
Mettam, C., Conneely, M.E. and White, S.J. (1994) Benthic macrofauna and sediments in the Severn Estuary. Biological Journal of the Linnean Society 51, 71–81.CrossRefGoogle Scholar
Morrisey, D.J., Sait, S.M., Little, C. and Wilson, R.S. (1994) The benthic ecology of river estuaries entering the Severn Estuary. Biological Journal of the Linnean Society 51, 247–251.CrossRefGoogle Scholar
Noël-Lambot, F., Bouquegneau, J.M., Frankenne, F. and Disteche, A. (1980) Cadmium, zinc and copper accumulation in limpets (Patella vulgata) from the Bristol Channel with special reference to metallothioneins. Marine Ecology Progress Series 2, 81–89.CrossRefGoogle Scholar
Owens, M. (1984) Severn Estuary—an appraisal of water quality. Marine Pollution Bulletin 15, 41–47.CrossRefGoogle Scholar
Poirier, L., Berthet, B., Amiard, J.C., Jeantet, A.Y. and Amiard-Triquet, C. (2006) A suitable model for the biomonitoring of trace metal bioavailabilities in estuarine sediments: the annelid polychaete Nereis diversicolor. Journal of the Marine Biological Association of the United Kingdom 86, 71–82.CrossRefGoogle Scholar
Potter, I.C., Claridge, P.N. and Warwick, R.M. (1986) Consistency of seasonal changes in an estuarine fish assemblage. Marine Ecology Progress Series 32, 217–228.CrossRefGoogle Scholar
Potter, I.C., Claridge, P.N., Hyndes, G.A. and Clarke, K.R. (1997) Seasonal, annual and regional variations in ichthyofaunal composition in the inner Severn Estuary and inner Bristol Channel. Journal of the Marine Biological Association of the United Kingdom 77, 507–525.CrossRefGoogle Scholar
Potter, I.C., Bird, D.J., Claridge, P.N., Clarke, K.R., Hyndes, G.A. and Newton, L.C. (2001) Fish fauna of the Severn Estuary. Are there long-term changes in abundance and species composition and are the recruitment patterns of the main marine species correlated? Journal of Experimental Marine Biology and Ecology 258, 15–37.CrossRefGoogle ScholarPubMed
Radford, P.J., Uncles, R.J. and Morris, A.W. (1981) Simulating the impact of technological change on dissolved cadmium distribution in the Severn Estuary. Water Research 15, 1045–1052.CrossRefGoogle Scholar
Rainbow, P.S. (1995) Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183–192.CrossRefGoogle Scholar
Riisgard, H.U., Kiorboe, T., Mohlenberg, F., Drabaek, I. and Madsen, P.P. (1985) Accumulation, elimination and chemical speciation of mercury in the bivalves Mytilus edulis and Macoma balthica. Marine Biology 86, 55–62.CrossRefGoogle Scholar
Rothery, P. (1988) A cautionary note on data transformation: bias in back-transformed means. Bird Study 35, 219–222.CrossRefGoogle Scholar
Scaps, P. (2002) A review of the biology, ecology and potential use of the common ragworm Hediste diversicolor (O.F. Müller) (Annelida: Polychaeta). Hydrobiologia 470, 203–218.CrossRefGoogle Scholar
Sokolowski, A., Wolowicz, M. and Hummel, H. (2007) Metal sources to the Baltic clam Macoma balthica (Mollusca: Bivalvia) in the southern Baltic Sea (the Gulf of Gdansk). Marine Environmental Research 63, 236–256.CrossRefGoogle Scholar
Sustainable Development Commission (2007a) Tidal power in the UK. Research report 3—review of Severn barrage proposals. London: Sustainable Development Commission, 250 pp.Google Scholar
Sustainable Development Commission (2007b) Turning the tide. Tidal power in the UK. London: Sustainable Development Commission, 148 pp.Google Scholar
Wang, W.X. and Fisher, N.S. (1999) Delineating metal accumulation pathways for marine invertebrates. Science of the Total Environment 238, 459–472.CrossRefGoogle Scholar
Wang, W.X. and Rainbow, P.S. (2005) Influence of metal exposure history on trace metal uptake and accumulation by marine invertebrates. Ecotoxicology and Environmental Safety 61, 145–159.CrossRefGoogle ScholarPubMed
Warwick, R.M. (1984) The benthic ecology of the Bristol Channel and Severn Estuary. Marine Pollution Bulletin 15, 70–75.CrossRefGoogle Scholar
Warwick, R.M. and Somerfield, P.J. (2010) The structure and functioning of the benthic macrofauna of the Bristol Channel and Severn Estuary, with predicted effects of a tidal barrage. Marine Pollution Bulletin 61, 92–99.CrossRefGoogle ScholarPubMed