Skip to main content

A review of the effects of heavy metals on freshwater mussels

The widespread recent decline in the species diversity and population density of freshwater mussels in North America may be partly related to chronic, low-level exposure to toxic metals. As benthic filter-feeding organisms, freshwater mussels are exposed to metals that are dissolved in water, associated with suspended particles and deposited in bottom sediments. Thus, freshwater mussels can bioaccumulate certain metals to concentrations that greatly exceed those dissolved in water. In adult mussels, the most common site of metal uptake is the gill, followed by the mantle and the kidney. The toxic effects of metals on freshwater mussels have been examined in a few acute toxicity tests, but the sublethal effects of long-term exposure to low environmental concentrations are little understood. Sublethal exposure to metals can alter growth, filtration efficiency, enzyme activity and behaviour. Sublethal effects are frequently observed at concentrations that are only half the lethal concentrations. However, few toxicity tests have used environmentally realistic exposure concentrations. Total concentrations of Cd, Cu, Hg and Zn in many oxic surface waters are in the ngl-1 range, yet many toxicity studies have exposed mussels to concentrations in the μgl-1 or even the mgl-1 range. An understanding of the processes by which metals affect freshwater mussels would provide insights on the ecotoxicological significance of metal contamination to natural mussel populations and aid in the development of water-quality criteria that adequately protect mussels.

This is a preview of subscription content, access via your institution.

References

  • Abolins-Krogis, A. (1958) The morphological and chemical characteristics of organic crystals in regenerating shells of Helix pomatia (L.). Acta Zool. (Stockholm) 39, 19–38.

    Google Scholar 

  • Adams, T.G., Atchison, G.J. and Vetter, R.J. (1981) The use of the three ridge clam (Amblema perplicata) to monitor trace metal contamination. Hydrobiologia 83, 67–72.

    Google Scholar 

  • Aldridge, D.W., Payne, B.S. and Miller, A.C. (1987) The effects of intermittent exposure to suspended solids and turbulence on three species of freshwater mussels. Environ. Pollut. 45, 17–28.

    Google Scholar 

  • Andersson, P. and Borg, H. (1988) Effects of liming on the distribution of cadmium in water, sediment, and organisms in a Swedish lake. Can. J. Fish. Aquat. Sci. 45, 1154–62.

    Google Scholar 

  • APHA (American Public Health Association), American Water Works Association and Water Pollution Control Federation (1989) Toxicity test procedures using mollusks. In Standard methods for the examination of water and wastewater, 17th edn, pp. 8–80. Washington, DC: American Public Health Association.

    Google Scholar 

  • ASTM (American Society for Testing and Materials) (1988) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. In Annual book of ASTM standards, Vol. 11.04, No. E 729–88, pp. 304–23. Philadelphia: American Society for Testing and Materials.

    Google Scholar 

  • Bates, J.M. (1982) The impact of impoundment on the mussel fauna of Kentucky Reservoir, Tennessee River. Am. Midl. Nat. 68, 232–6.

    Google Scholar 

  • Bayne, B.L., Widdows, J. and Newell, R.I.E. (1977) Physiological measurements on estuarine bivalve molluscs in the field. In Keenen, B.F., O'Ceidigh, P. and Boaden, P.J.S. eds. Biology of benthic organisms, pp. 57–68. New York: Pergamon Press.

    Google Scholar 

  • Bayne, B.L., Brown, D.A., Burns, K., Dixon, D.R., Ivanovici, A., Livingstone, D.R., Lowe, D.M., Moore, M.N., Stebbing, A.R.D. and Widdows, J. (1985) The Effects of Stress and Pollution on Marine Animals. New York: Praeger Scientific.

    Google Scholar 

  • Becker, G.L., Chen, C.H., Greenawalt, J.W. and Lehninger, A.L. (1974) Calcium phosphate granules in the hepatopancreas of the blue crab Callinectes sapidus. J. Cell Biol. 61, 316–26.

    Google Scholar 

  • Belanger, S.E., Farris, J.L., Cherry, D.S. and Cairns, J. Jr (1986) Growth of Asiatic clams (Corbicula sp.) during and after long-term zinc exposure in field-located and laboratory artificial streams. Arch. Environ. Contam. Toxicol. 15, 427–34.

    Google Scholar 

  • Bias, R. and Karbe, L. (1985) Bioaccumulation and partitioning of cadmium within the freshwater mussel Dreissena polymorpha Pallas. Int. Rev. Gesamten Hydrobiol. 70, 113–25.

    Google Scholar 

  • Bloom, N.S. and Effler, S.W. (1990) Seasonal variability in the mercury speciation of Onondaga Lake (New York). Water Air Soil Pollut. 53, 251–65.

    Google Scholar 

  • Borchardt, T.H. (1983) The influence of food quantity on the kinetics of cadmium uptake and loss via food and seawater in Mytilus edulis. Mar. Biol. 76, 67–76.

    Google Scholar 

  • Borg, H. (1987) Trace metals and water chemistry of forest lakes in Northern Sweden. Water Res. 21, 65–72.

    Google Scholar 

  • Bryan, G.W. and Uysal, H. (1978) Heavy metals in the burrowing bivalve Scrobicularia plana from the Tamar Estuary in relation to environmental levels. J. Mar. Biol. Assoc. UK 58, 89–108.

    Google Scholar 

  • Buchanan, J.B., Brown, B.E., Coombs, T.L., Pirie, B.J.S. and Allen, J.A. (1980) The accumulation of ferric iron in the guts of some spatangoid echinoderms. J. Mar. Biol. Assoc. UK 60, 631–40.

    Google Scholar 

  • Cameron, C.J., Cameron, I.F. and Paterson, C.G. (1979) Contribution of organic shell matter to biomass estimates of unionid bivalves. Can. J. Zool. 57, 1666–9.

    Google Scholar 

  • Campbell, P.G.C. and Tessier, A. (1987) Metal species in natural waters: influence of environmental acidification. In Hites, R.A. and Eisenreich, S.J. eds. Sources and fates of aquatic pollutants, Advanced Chemical Series 216, Chapter 7, pp. 185–207. Washington, DC: American Chemical Society.

    Google Scholar 

  • Carmichael, N.G., Squibb, K.S. and Fowler, B.A. (1979) Metals in the molluscan kidney: a comparison of two closely related bivalve species (Argopecten), using X-ray microanalysis and atomic absorption spectrophotometry. J. Fish. Res. Board Can. 36, 1149–55.

    Google Scholar 

  • Cassini, A., Tallandini, L., Favero, N. and Albergoni, V. (1986) Cadmium bioaccumulation studies in the freshwater molluscs Anodonta cygnea and Unio elongatulus. Comp. Biochem. Physiol. 84C, 35–41.

    Google Scholar 

  • Coale, K.H. and Flegal, A.R. (1989) Copper, zinc, cadmium, and lead in surface waters of Lakes Erie and Ontario. Sci. Total Environ. 87/88, 297–304.

    Google Scholar 

  • Coon, T.G., Eckblad, J.W. and Trygstad, P.M. (1977) Relative abundance and growth of mussels in pools 8, 9 and 10 of the Mississippi River. Freshwater Biol. 7, 279–85.

    Google Scholar 

  • Couillard, Y., Campbell, P.G.C. and Tessier, A. (1993) Response of metallothionein concentrations in a freshwater bivalve (Anodonta grandis) along an environmental cadmium gradient. Limnol. and Oceanogr. 38, 299–313.

    Google Scholar 

  • Cunningham, P.A. (1979) The use of bivalve molluscs in heavy metal pollution research. In Vernberg, W.B., Calabrese, A., Thurnberg, F. and Thurnberg, F.J. eds. Marine pollution: functional responses, pp. 183–221. New York: Academic Press.

    Google Scholar 

  • Doherty, F.G. and Cherry, D.S. (1988) Tolerance of the Asiatic clam Corbicula spp. to lethal levels of toxic stressors — a review. Environ. Pollut. 51, 269–313.

    Google Scholar 

  • Doherty, F.G., Cherry, D.S. and Cairns, J. Jr (1987) Valve closure responses of the Asiatic clam Corbicula fluminea exposed to cadmium and zinc. Hydrobiologia 153, 159–67.

    Google Scholar 

  • Ellis, M.M. (1929) The artificial propagation of freshwater mussels. Trans. Am. Fish. Soc. 59, 217–23.

    Google Scholar 

  • Ellis, M.M. (1936) Erosion silt as a factor in aquatic environments. Ecology 17, 29–42.

    Google Scholar 

  • Farris, J.L., Van Hassel, J.H., Belanger, S.E., Cherry, D.S. and Cairns, J. Jr (1988) Application of cellulolytic activity of Asiatic clams (Corbicula sp.) to in-stream monitoring of power plant effluents. Environ. Toxicol. Chem. 7, 701–13.

    Google Scholar 

  • Forstner, U. and Wittmann, G.T.W. (1981) Metal Pollution in the Aquatic Environment. Berlin: Springer-Verlag.

    Google Scholar 

  • Fuller, S.L.H. (1974) Clams and mussels (Mollusca: Bivalvia). In Hart, C.W. Jr and Fuller, S.L.H. eds. Pollution ecology of freshwater invertebrates, pp. 213–73. New York: Academic Press.

    Google Scholar 

  • Garvey, J.S. (1990) Metallothionein: a potential biomarker of exposure to environmental toxins. In McCarthy, J.F. and Shugart, L.R. eds. Biomarkers of environmental contamination, pp 267–87. Chelsea: Lewis Publishers.

    Google Scholar 

  • George, S.G. and Pirie, B.J.S. (1979) The occurrence of cadmium in subcellular particles in the kidney of the marine mussel, Mytilus edulis, exposed to cadmium. The use of electron microprobe analysis. Biochim. Biophys. Acta 580, 234–44.

    Google Scholar 

  • Giesy, J.P. and Hoke, R.A. (1989) Freshwater sediment toxicity bioassessment: rationale for species selection and test design. J. Great Lakes Res. 15, 539–69.

    Google Scholar 

  • Gill, G.A. and Bruland, K.W. (1990) Mercury speciation in surface freshwater systems in California and other areas. Environ. Sci. Technol. 24, 1392–400.

    Google Scholar 

  • Gill, G.A. and Bruland, K.W. (1992) Mercury Speciation and Cycling in a Seasonally Anoxic Freshwater System: Davis Creek Reservoir. Palo Alto, CA: Final Report to Electric Power Research Institute.

  • Goldberg, E.D., Bowen, V.T., Farrington, J.W., Harvey, G., Martin, J.H., Parker, P.L., Risebrough, R.W., Robertson, W., Schneider, E. and Gamble, E. (1978) The mussel watch. Environ. Conservat. 5, 101–25.

    Google Scholar 

  • Gordon, M.E. and Layzer, J.B. (1989) Mussels (Bivalvia: Unionoida) of the Cumberland River: a review of life histories and ecological relationships. US Fish Wildl. Service Biol. Rep. 89 (15).

  • Green, R.H. (1980) Role of a unionid clam population in the calcium budget of a small arctic lake. Can. J. Fish. Aquat. Sci. 37, 219–24.

    Google Scholar 

  • Green, W.J., Canfield, D.E., Lee, F.G. and Jones, A.R. (1986) Mn, Fe, Cu, and Cd distributions and residence times in closed basin Lake Vanda (Wright Valley, Antarctica). Hydrobiologia 134, 237–48.

    Google Scholar 

  • Guary, J.C. and Negrel, R. (1981) Calcium phosphate granules: a trap for transuranics and iron in crab hepatopancreas. Comp. Biochem. Physiol. 68A, 423–7.

    Google Scholar 

  • Hamilton, S.J. and Mehrle, P.M. (1986) Metallothionein in fish: review of its importance in assessing stress from metal contaminants. Trans. Am. Fish. Soc. 115, 596–609.

    Google Scholar 

  • Harrison, F.L., Knezovich, J.P. and Rice, D.W. Jr (1984) The toxicity of copper to the adult and early life stages of the freshwater clam, Corbicula manilensis. Arch. Environ. Contam. Toxicol. 13, 85–92.

    Google Scholar 

  • Hemelraad, J. and Herwig, H.J. (1988) Cadmium kinetics in freshwater clams. IV. Histochemical localization of cadmium in Anodonta cygnea and Anodonta anatina exposed to cadmium chloride. Arch. Environ. Contam. Toxicol. 17, 333–43.

    Google Scholar 

  • Hemelraad, J., Holwerda, D.A., Teerds, K.J., Herwig, H.J. and Zandee, D.I. (1986a) Cadmium kinetics in freshwater clams. II. A comparative study of cadmium uptake and cellular distribution in the Unionidae Anodonta cygnea, Anodonta anatina, and Unio pictorum. Arch. Environ. Contam. Toxicol. 15, 9–21.

    Google Scholar 

  • Hemelraad, J., Holwerda, D.A. and Zandee, D.I. (1986b) Cadmium kinetics in freshwater clams. I. The pattern of cadmium accumulation in Anodonta cygnea. Arch. Environ. Contam. Toxicol. 15, 1–7.

    Google Scholar 

  • Hemelraad, J., Kleinveld, H.A., de Roos, A.M., Holwerda, D.A. and Zandee, D.I. (1987) Cadmium kinetics in freshwater clams. III. Effects of zinc on uptake and distribution of cadmium in Anodonta cygnea. Arch. Environ. Contam. Toxicol. 16, 95–101.

    Google Scholar 

  • Herwig, H.J. (1989) Effects of cadmium on valve-gape patterns of a freshwater bivalve. In Vernet, J.P. ed. Proceedings of an international conference: Heavy Metals in the Environment, pp. 566–9. Edinburgh: CEP Consultants.

    Google Scholar 

  • Herwig, H.J., Brands, F., Kruitwagen, E. and Zandee, D.I. (1989) Bioaccumulation and histochemical localization of cadmium in Dreissena polymorpha exposed to cadmium chloride. Aquat. Toxicol. 15, 269–86.

    Google Scholar 

  • Holwerda, D.A., Hemelraad, J., Veenhof, P.R. and Zandee, D.I. (1988) Cadmium accumulation and depuration in Anodonta anatina exposed to cadmium chloride or cadmium-EDTA complex. Bull. Environ. Contam. Toxicol. 40, 373–80.

    Google Scholar 

  • Holwerda, D.A., deKnecht, J.A., Hemelraad, J. and Veenhof, P.R. (1989) Cadmium kinetics in freshwater clams. Uptake of cadmium by the excised gill of Anodonta anatina. Bull. Environ. Contam. Toxicol. 42, 382–8.

    Google Scholar 

  • Huynh-Ngoc, L., Whitehead, N.E. and Oregioni, B. (1988a) Cadmium in the Rhone River. Water Res. 22, 571–6.

    Google Scholar 

  • Huynh-Ngoc, L., Whitehead, N.E. and Oregioni, B. (1988b) Low levels of copper and lead in a highly industrialized river. Toxicol. Environ. Chem. 17, 223–36.

    Google Scholar 

  • Imlay, M.J. (1968) Environmental factors in activity rhythms of the freshwater clam Elliptio complanatus catawbensis (Lea). Am. Midl. Nat. 80, 508–28.

    Google Scholar 

  • Isom, B.G. (1969) The mussel resource of the Tennessee River. Malacologia 7, 397–425.

    Google Scholar 

  • Isom, B.G. and Hudson, R.G. (1982) In vitro culture of parasitic freshwater mussel glochidia. Nautilus 96, 147–51.

    Google Scholar 

  • Isom, B.G. and Yokley, P. Jr (1968) The mussel fauna of Duck River in Tennessee, 1965. Am. Midl. Nat. 80, 34–42.

    Google Scholar 

  • Ivlev, V.S. (1961) Experimental Ecology of the Feeding of Fishes. New Haven: Yale University Press.

    Google Scholar 

  • Jacobson, P.J., Farris, J.L. and Cherry, D.S. (1993) Juvenile freshwater mussel (Bivalvia: Unionidae) responses to acute toxicity testing with copper. Environ. Toxicol. Chem. 12, 879–83.

    Google Scholar 

  • Janssen, H.H. and Scholz, N. (1979) Uptake and cellular distribution of cadmium in Mytilus edulis. Mar. Biol. 55, 133–41.

    Google Scholar 

  • Keller, A.E. and Zam, S.G. (1991) The acute toxicity of selected metals to the freshwater mussel, Anodonta imbecilis. Environ. Toxicol. Chem. 10, 539–46.

    Google Scholar 

  • Lasee, B.A. (1991) Histological and ultrastructural studies of larval and juvenile Lampsilis (Bivalvia) from the upper Mississippi River. PhD Dissertation, Iowa State University, Ames, IA.

    Google Scholar 

  • Lee, H. (1991) A clam's eye view of the bioavailability of sediment-associated pollutants. In Baker, R.A. ed. Organic substances and sediments in water, pp. 73–93. Chelsea: Lewis Publishers.

    Google Scholar 

  • Lee, Y.H. and Iverfeldt, Å. (1991) Measurement of methylmercury and mercury in run-off, lake and rain waters. Water Air Soil Pollut. 56, 309–21.

    Google Scholar 

  • Leland, H.V. and Kuwabara, J.S. (1985) Trace metals. In Rand, G.M. and Petrocelli, S.R. eds. Fundamentals of aquatic toxicology, pp. 374–415. Washington, DC: Hemisphere Publishing Company.

    Google Scholar 

  • Luoma, S.N. and Bryan, G.W. (1978) Factors controlling the availability of sediment-bound lead to the estuarine bivalve Scrobicularia plana. J. Mar. Biol. Assoc. UK 58, 793–802.

    Google Scholar 

  • Luoma, S.N. and Bryan, G.W. (1979) Trace metal bioavailability: modeling chemical and biological interactions of sediment-bound Zn. In Jenne, E.A. ed. Chemical modeling in aqueous systems, ACS Symposium Series 93, pp. 577–609. Washington, DC: American Chemical Society.

    Google Scholar 

  • Luoma, S.N. and Jenne, E.A. (1976) Factors affecting the availability of sediment-bound cadmium to the estuarine deposit feeding clam, Macoma balthica. In Cushing, C.E. Jr ed. Radioecology and energy resources, pp. 283–91. Stroudsberg: Hutchinson and Ross, Inc.

    Google Scholar 

  • Luoma, S.N. and Jenne, E.A. (1977) The availability of sediment-bound cobalt, silver, and zinc to a deposit-feeding clam. In Wildung, R.E. and Drucker, H. eds. Biological implications of metals in the environment, CONF-750929, pp. 213–31. Springfield: National Technical Information Center.

    Google Scholar 

  • McCall, P.I., Tevesz, M.J.S. and Schwelgien, S.F. (1979) Sediment mixing by Lampsilis radiata siliquoidea (Mollusca) from western Lake Erie. J. Great Lakes Res. 5, 105–11.

    Google Scholar 

  • McMahon, R.F. (1991) Mollusca: Bivalvia. In Thorp, J.H. and Covich, A.P. eds. Ecology and classification of North American freshwater invertebrates, pp. 315–39. New York: Academic Press.

    Google Scholar 

  • Mackie, G.L. (1991) Biology of the exotic zebra mussel, Dreissena polymorpha, in relation to native bivalves and its potential impact in Lake St. Clair. Hydrobiologia 219, 251–68.

    Google Scholar 

  • Manly, R. and George, W.O. (1977) The occurrence of some heavy metals in populations of the freshwater mussel Anodonta anatina (L.) from the River Thames. Environ. Pollut. 14, 139–54.

    Google Scholar 

  • Mann, K.H. (1964) The pattern of energy flow in the fish and invertebrate fauna of the River Thames. Verhandlungen der Internationalen Vereinigung fur Theoretische Angewandte Limnologie 15, 485–95.

    Google Scholar 

  • Marshall, A.T. and Talbot, V. (1979) Accumulation of cadmium and lead in the gills of Mytilus edulis: X-ray microanalysis and chemical analysis. Chemico-Biological Interactions 27, 111–23.

    Google Scholar 

  • Millington, P.J. and Walker, K.F. (1983) Australian freshwater mussel Velesunio ambiguus (Philippi) as a biological monitor for zinc, iron and manganese. Aust. J. Mar. Freshwater Res. 34, 873–92.

    Google Scholar 

  • Mitchell, L.G., Mutchmor, J.A. and Dolphin, W.D. (1988) Zoology. Menlo Park: The Benjamin Cummings Publishing Company.

    Google Scholar 

  • Moore, J.W. and Ramamoorthy, S. (1984) Heavy Metals in Natural Waters: Applied Monitoring and Impact Assessment. New York: Springer-Verlag.

    Google Scholar 

  • Morgan, E.L., Yokley, P. Jr, Rausina, G., Wright, J.R. Jr, McFadden, J.F. and Red, J.T. (1989) A toxicity test protocol for mature bivalve mussels using automated biological monitoring. In Weigmann, D.L. ed. Proceedings of the National Research Conference on Pesticides in Terrestrial and Aquatic Environments, pp. 259–64. Blacksburg: Virginia Polytechnic Institute and State University.

    Google Scholar 

  • Naimo, T.J., Atchison, G.J. and Holland-Bartels, L.E. (1992a) Sublethal effects of cadmium on physiological responses in the pocketbook mussel, Lampsilis ventricosa. Environ. Toxicol. Chem. 11, 1013–21.

    Google Scholar 

  • Naimo, T.J., Waller, D. and Holland-Bartels, L.E. (1992b) Heavy metals in the threeridge mussel Amblema plicata plicata (Say, 1817) in the Upper Mississippi River. J. Freshwater Ecol. 7, 209–18.

    Google Scholar 

  • Negus, C.L. (1966) A quantitative study of growth and reproduction of unionid mussels in the River Thames at Reading. J. Anim. Ecol. 35, 513–32.

    Google Scholar 

  • neves, R.J. and Widlak, J.C. (1987) Habitat ecology of juvenile freshwater mussels (Bivalvia: Unionidae) in a headwater stream in Virginia. Am. Malacol. Bull. 5, 1–7.

    Google Scholar 

  • Norton, S.A., Dillon, P.J., Evans, R.D., Mierle, G. and Kahl, J.S. (1990) The history of atmospheric deposition of Cd, Hg, and Pb in North America: evidence from lake and peat bog sediments. In Lindberg, S.E., Page, A.L. and Norton, S.A. eds. Sources, deposition, and canopy interactions, Vol. 3, Acidic precipitation, pp. 73–102. New York: Springer-Verlag.

    Google Scholar 

  • Nriagu, J.O., Pfeiffer, W.C., Malm, O., Souza, C.M.M. and Mierle, G. (1992) Mercury pollution in Brazil. Nature (London) 356, 389.

    Google Scholar 

  • Nriagu, J.O., Lawson, G., Wong, H.K.T. and Azcue, J.M. (1993) A protocol for minimizing contamination in the analysis of trace metals in Great Lakes waters. J. Great Lakes Res. 19, 175–82.

    Google Scholar 

  • Paloheimo, J.E. and Dickie, L.M. (1966) Food and growth of fishes. III. Relations among food, body size and growth efficiency. J. Fish. Res. Board Can. 23, 869–908.

    Google Scholar 

  • Pauley, G.B. and Nakatini, R.E. (1968) Metabolism of the radioisotope 65Zn in the freshwater mussel Anodonta californiensis. J. Fish. Res. Board Can. 25, 2691–4.

    Google Scholar 

  • Pennak, R.W. (1978) Fresh-water Invertebrates of the United States. New York: Wiley and Sons.

    Google Scholar 

  • Phillips, D.J.H. (1977) The use of biological indicator organisms to monitor trace metal pollution in marine and estuarine environments — a review. Environ. Pollut. 13, 281–317.

    Google Scholar 

  • Pynnonen, K., Holwerda, D.A. and Zandee, D.I. (1987) Occurrence of calcium concretions in various tissues of freshwater mussels and their capacity for cadmium sequestration. Aquat. Toxicol. 10, 101–14.

    Google Scholar 

  • Rada, R.G., Wiener, J.G., Winfrey, M.R. and Powell, D.E. (1989) Recent increases in atmospheric deposition of mercury to North-Central Wisconsin lakes inferred from sediment analyses. Arch. Environ. Contam. Toxicol. 18, 175–81.

    Google Scholar 

  • Rada, R.G., Wiener, J.G., Bailey, P.A. and Powell, D.E. (1990) Recent influexes of metals into Lake Pepin, a natural lake on the Upper Mississippi River. Arch. Environ. Contam. Toxicol. 19, 712–16.

    Google Scholar 

  • Ramsey, D.J. (1990) Measurements of Methylation Balance in Southern Indian Lake, Granville Lake, and Stephens Lake, Manitoba, 1989. Winnipeg, Manitoba: Environment Canada, Fisheries and Oceans, Northern Flood Agreement, Ecological Report 90-3, p 89.

  • Ravera, O. (1984) Cadmium in freshwater ecosystems. Experientia 40, 2–14.

    Google Scholar 

  • Ray, S. (1984) Bioaccumulation of cadmium in marine organisms. Experientia 40, 14–23.

    Google Scholar 

  • Ringwood, A.H. (1990) The relative sensitivities of different life stages of Isognomon californicum to cadmium toxicity. Arch. Environ. Contam. Toxicol. 19, 338–40.

    Google Scholar 

  • Robinson, W.E. and Ryan, D.K. (1986) Metal interactions within the kidney, gill, and digestive gland of the hard clam Mercenaria, following laboratory exposure to cadmium. Arch. Environ. Contam. Toxicol. 15, 23–30.

    Google Scholar 

  • Rodgers, J.H., Cherry, D.S., Graney, R.L., Dickson, K.L. and Cairns, J. Jr (1980) Comparison of heavy metal interactions in acute and artificial bioassay techniques for the Asiatic clam (Corbicula fluminea). In Eaton, J.G., Parish, P.R. and Hendricks, A.C. eds. Aquatic toxicology, ASTM STP 707, pp. 266–80. Philadelphia: American Society for Testing and Materials.

    Google Scholar 

  • Rognerud, S. and Fjeld, E. (1993) Regional survey of heavy metals in lake sediments in Norway. Ambio 22, 206–12.

    Google Scholar 

  • Russell-Hunter, W.D., Aldridge, D.A., Tashiro, J.S. and Payne, B.S. (1983) Oxygen uptake and nitrogenous excretion rates during overwinter degrowth conditions in the pulmonate snail, Helisoma trivolvis. Comp. Biochem. Physiol. 74A, 491–7.

    Google Scholar 

  • Salanki, J. and Varanka, I. (1976) Effect of copper and lead compounds on the activity of the freshwater mussel. Ann. Inst. Biol. (Tihany) Hungaricae Acad. Sci. 43, 21–7.

    Google Scholar 

  • Salomons, W. and Forstner, U. (1984) Metals in the Hydrocycle. Berlin: Springer-Verlag.

    Google Scholar 

  • Salomons, W., de Rooij, N.M., Kerdijk, H. and Bril, J. (1987) Sediments as a source for contaminants. Hydrobiologia 149, 13–30.

    Google Scholar 

  • Schmitt, C.J., Finger, S.E., May, T.W. and Kaiser, M.S. (1987) Bioavailability of lead and cadmium from mine tailings to the pocketbook mussel (Lampsilis ventricosa). In Neves, R.J. ed. Proceedings of the Die-offs of freshwater mussels in the United States Workshop, pp. 115–42. Davenport: US Fish and Wildlife Service and the Upper Mississippi River Conservation Committee.

    Google Scholar 

  • Shiller, A.M. and Boyle, E. (1985) Dissolved zinc in rivers. Nature 317, 49–52.

    Google Scholar 

  • Silverman, H., Steffens, W.L. and Dietz, T.H. (1985) Calcium from extracellular concretions in the gills of freshwater unionid mussels is mobilized during reproduction. J. Exp. Zool. 236, 137–47.

    Google Scholar 

  • Silverman, H., Todd Kays, W. and Dietz, T.H. (1987a) Maternal calcium contribution to glochidial shells in freshwater mussels (Eulamellibranchia: Unionidae). J. Exp. Zool. 242, 137–46.

    Google Scholar 

  • Silverman, H., McNeil, J.W. and Dietz, T.H. (1987b) Interaction of trace metals, Zn, Cd, and Mn with Ca concretions in the gills of freshwater unionid mussels. Can. J. Zool. 65, 828–32.

    Google Scholar 

  • Simkiss, K. (1981) Cellular discrimination processes in metal accumulating cells. J. Exp. Biol. 94, 317–27.

    Google Scholar 

  • Sloof, W., de Zwart, D. and Marquenie, J.M. (1983) Detection limits of a biological monitoring system for chemical water pollution based on mussel activity. Bull. Environ. Contam. Toxicol. 30, 400–5.

    Google Scholar 

  • Spry, D.J. and Wiener, J.G. (1991) Metal bioavailability and toxicity to fish in low-alkalinity lakes: a critical review. Environ. Pollut. 71, 243–304

    Google Scholar 

  • Stanczykowska, A., Lawacz, W., Mattice, J. and Lewandowski, K. (1976) Bivalves as a factor affecting the circulation of matter in Lake Mikolajskie (Poland). Limnologica 10, 347–52.

    Google Scholar 

  • Stansbery, D.H. (1970) A Study of the Growth Rate and Longevity of the Naiad Amblema plicata (Say, 1817) in Lake Erie (Bivalvia: Unionidae). American Malacological Union Incorporated Annual Reports.

  • Starrett, W.C. (1971) A survey of the mussels (Unionacea) of the Illinois River: a polluted stream. Illinois Nat. History Survey Bull. 30.

  • Steinert, S.A. and Pickwell, G.V. (1988) Expression of heat shock proteins and metallothionein in mussels exposed to heat stress and metal ion challenge. Mar. Environ. Res. 24, 211–14.

    Google Scholar 

  • Taylor, H.E., Garbarino, J.R. and Brinton, T.I. (1990) The occurrence and distribution of trace metals in the Mississippi River and its tributaries. Sci. Total Environ. 97/98, 369–84.

    Google Scholar 

  • Tessier, A. and Campbell, P.G.C. (1987) Partitioning of trace metals in sediments: relationships with bioavailability. Hydrobiologia 149, 43–52.

    Google Scholar 

  • Tessier, A., Campbell, P.G.C., Auclair, J.C. and Bisson, M. (1984) Relationships between the partitioning of trace metals in sediments and their accumulation in the tissue of the freshwater mollusc Elliptio complanata in a mining area. Can. J. Fish. Aquat. Sci. 41, 1463–77.

    Google Scholar 

  • Tessier, A., Couillard, Y., Campbell, P.G.C. and Auclair, J.C. (1993) Modeling Cd partitioning in oxic lake sediments and Cd concentrations in the freshwater bivalve Anodonta grandis. Limnol. Oceanogr. 38, 1–17.

    Google Scholar 

  • Thompson, R.J. and Bayne, B.L. (1974) Some relationships between growth, metabolism and food in the mussel Mytilus edulis. Mar. Biol. 27, 317–26.

    Google Scholar 

  • Trefry, J.H., Nelsen, T.A., Trocine, R.P., Metz, S. and Vetter, T.W. (1986) Trace metal fluxes through the Mississippi River Delta system. Rapport et Proces-Verbaux des Reunions Conseil International pour l'Exploration de la Mer 186, 277–88.

    Google Scholar 

  • US Environmental Protection Agency (1984) Ambient Water Quality Criteria for Copper. EPA/440/5–84/031. Washington, DC: US Environmental Protection Agency.

    Google Scholar 

  • Van der Schalie, H. and Van der Schalie, A. (1950) The mussels of the Mississippi River. Am. Midl. Nat. 44, 448–66.

    Google Scholar 

  • Viarengo, A., Zanicchi, G., Moore, M.N. and Orunesu, M. (1981) Accumulation and detoxication of copper by the mussel Mytilus galloprovincialis, Lam.: a study of the subcellular distribution in the digestive gland cells. Aquat. Toxicol. 1, 147–57.

    Google Scholar 

  • Waalkes, M.P. and Poirier, L.A. (1984) In vitro cadmium-DNA interactions: cooperativity of cadmium binding and competitive antagonism by calcium, magnesium and zinc. Toxicol. Appl. Pharmacol. 75, 539–46.

    Google Scholar 

  • Walker, G. (1977) "Copper" granules in the barnacle Balanus balanoides. Mar. Biol. 39, 342–9.

    Google Scholar 

  • Walker, G., Rainbow, P.S., Foster, P. and Holland, D.L. (1975) Zinc phosphate granules in tissue surrounding the midgut of the barnacle Balanus balanoides. Mar. Biol. 33, 161–6.

    Google Scholar 

  • Widdows, J. (1978) Physiological indices of stress in Mytilus edulis. J. Mar. Biol. Assoc. UK 58, 125–42.

    Google Scholar 

  • Widdows, J., Phelps, D.K. and Galloway, W. (1981) Measurement of physiological condition of mussels transplanted along a pollution gradient in Narragansett Bay. Mar. Environ. Res. 4, 181–94.

    Google Scholar 

  • Williams, J.C. and Schuster, G.A. (1989) Freshwater Mussel Investigations of the Ohio River. Mile 317.0 to 981.0. Frankfort: Division of Fisheries, Kentucky Department of Fish and Wildlife Resources.

    Google Scholar 

  • Winberg, R.G. (1960) Rate of metabolism and food requirements of fishes. Fish. Res. Board Can. Transl. Series 194.

  • Windom, H.L., Byrd, J.T., Smith, R.G. Jr and Huan, F. (1991) Inadequacy of NASQAN data for assessing metal trends in the nation's rivers. Environ. Sci. Technol. 25, 1137–42.

    Google Scholar 

  • Yeager, M.M. and Cherry, D.S. (1994) Feeding and burrowing behaviors of juvenile rainbow mussels, Villosa iris (Bivalvia: Unionidae). J. N. Am. Benthol. Soc. 13, 217–22.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Naimo, T.J. A review of the effects of heavy metals on freshwater mussels. Ecotoxicology 4, 341–362 (1995). https://doi.org/10.1007/BF00118870

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00118870

Keywords

  • freshwater mussels
  • metals
  • effects
  • bioaccumulation
  • toxicity
  • review