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Variables affecting body burdens of lead, zinc and cadmium in a roadside population of the snailCepaea hortensis Müller

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Application of multiple regression analysis to the lead, zinc and cadmium contents of 985Cepaea hortensis collected from a suburban roadside site over two years showed that body weight, age and daylength were the major factors affecting soft tissue body burdens. Other highly significant influences were physiological changes at the juvenile-adult transition, vapour pressure deficit for the two days before sampling, and mean rainfall for the ten days before. Together these factors accounted for 69%, 79% and 87% of the total variance in lead, zinc and cadmium body burdens respectively. Unexplained variance was provisionally ascribed to individual differences in recent diet and digestive activity. The digestive gland contined the majority of the total body burden of each metal and played an important role in lead and zinc elimination. Whereas levels of lead inC. hortensis fluctuated rapidly, zinc was exchanged more slowly, perhaps by active regulation, and cadmium was effectively immobile, accumulating progressively with age. The implications of these results to the predators of land snails, and to terrestrial monitoring programmes, are discussed.

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  1. Anderson, R.V.: Concentrations of cadmium, copper, lead, and zinc in six species of freshwater clams. Bull. Environ. Contam. toxicol.18, 492–496 (1977)

  2. Bailey, S.E.R.: The seasonal and daily patterns of locomotor activity in the snailHelix aspersa Müller, and their relation to environmental variables. Proc. malac. Soc. Lond.41, 415–428 (1975)

  3. Bilham, E.G.: The Climate of the British Isles. London: Macmillan (1938)

  4. Boyden, C.R.: Trace element content and body size in molluscs. Nature (Lond.)251, 311–314 (1974)

  5. Boyden, C.R.: Effect of size upon metal content of shellfish. J. mar. biol. Ass. U.K.57, 675–714 (1977)

  6. Bryan, G.W.: The occurrence and seasonal variation of trace metals in the scallopsPecten maximus (L.) andChlamys opercularis (L.). J. mar. biol. Ass. U.K.53, 145–166 (1973)

  7. Bryan, G.W., Uysal, H.: Heavy metals in the burrowing bivalveScrobicularia plana from the Tamar estuary in relation to environmental levels. J. mar. biol. Ass. U.K.58, 89–108 (1978)

  8. Butler, P.A., Andrén, L., Bonde, G.J., Jernelöv, A., Reisch, D.J.: Monitoring organisms. F.A.O. Fisheries Reports, No. 99, Supplement1, 101–112 (1971)

  9. Cain, A.J., Currey, J.D.: Studies onCepaea. III. Ecogenetics of a population ofCepaea nemoralis (L.) subject to strong area effects. Phil. Trans. R. Soc. Lond. B.253, 447–482 (1968)

  10. Cameron, R.A.D.: The effect of temperature on the activity of three species of Helicid snail (Mollusca: Gastropoda). J. Zool., Lond.162, 303–315 (1970)

  11. Cameron, R.A.D., Williamson, P.: Estimating migration and the effects of disturbance in mark-recapture studies on the snailCepaea nemoralis L. J. Anim. Ecol.46, 173–179 (1977)

  12. Cannon, H.L., Anderson, B.M.: The geochemists' involvement with the pollution problem. Geol. Soc. Am., Memoir123, 155–177 (1971)

  13. Cannon, H.L., Bowles, J.M.: Contamination of vegetation by tetraethyl lead. Science137, 765–766 (1962)

  14. Carter, M.A.: Thrush predation of an experimental population of the snailCapaea nemoralis (L.). Proc. Linn. Soc. Lond.179, 241–249 (1968)

  15. Chow, T.J.: Lead accumulation in roadside soil and grass. Nature (Lond.)225, 295–296 (1970)

  16. Clarke, J.H., Clarke, A.N., Wilson, D.J.: Lead levels in freshwater mollusk shells. J. Environ. Sci. Health11, 65–78 (1976)

  17. Coombs, T.L.: The distribution of zinc in the oysterOstrea edulis and its relation to enzymic activity and to other metals. Mar. Biol.12, 170–178 (1972)

  18. Coombs, T.L.: The nature of zinc and copper complexes in the oysterOstrea edulis. Mar. Biol.28, 1–10 (1974)

  19. Coughtrey, P.J., Martin, M.H.: The distribution of Pb, Zn, Cd and Cu within the pulmonate molluscHelix asparsa Müller. Oecologia (Berl.)23, 315–322 (1976a)

  20. Coughtrey, P.J., Martin, M.H.: A comment on the analysis of biological materials for lead using atomic absorption spectroscopy. Chemosphere5, 183–186 (1976b)

  21. Coughtrey, P.J., Martin, M.H.: The uptake of lead, zinc, cadmium, and copper by the pulmonate mollusc,Helix aspersa Müller, and its relevance to the monitoring of heavy metal contamination of the environment. Oecologia (Berl.)27, 65–74 (1977)

  22. Darracott, A., Watling, H.: The use of molluscs to monitor cadmium levels in estuaries and coastal marine environments. Trans. roy. Soc. S. Afr.41, 325–338 (1975)

  23. Davies, B.E., Holmes, P.L.: Lead contamination of roadside soil and grass in Birmingham, England, in relation to naturally occurring levels. J. agric. Sci. Camb.79, 479–484 (1972)

  24. Durham University Observatory: Daily Meterological Observations. Dept. of Geography, University of Durham 1975–1977

  25. Fagerström, T.: Body weight, metabolic rate, and trace substance turnover in animals. Oecologia (Berl.)29, 99–104 (1977)

  26. Frazier, J.M.: The dynamics of metals in the American oyster,Crassostrea virginica. I. Seasonal effects. Chesapeake Science16, 162–171 (1975)

  27. Free, J.B., Gennard, D., Stevenson, J.H., Williams, I.H.: Beneficial insects present on a motorway verge. Biol. Conserv.8, 61–72 (1975)

  28. Giles, F.E., Middleton, S.G., Grau, J.G.: Evidence for accumulation of atmospheric lead by insects in areas of high traffic density. Environ. Entomol.2, 299–300 (1973)

  29. Gish, C.D., Christensen, R.E.: Cadmium, nickel, lead and zinc in earthworms from roadside soil. Environ. Sci. Technol.7, 1060–1062 (1973)

  30. Goldsmith, C.D., Scanlon, P.F.: Lead levels in small mammals and selected invertebrates associated with highways of different traffic densities. Bull. Environ. Contam. Toxicol.17, 311–316 (1977)

  31. Ireland, M.P.: Metal content ofDendrobaena rubida (Oligochaeta) in a base metal mining area. Oikos26, 74–79 (1975)

  32. Ireland, M.P.: Lead retention in toadsXenopus laevis fed increasing levels of lead-contaminated earthworms. Environ. Pollut.12, 85–92 (1977)

  33. Ireland, M.P., Wootton, R.J.: Variations in the lead, zinc and calcium content ofDendrobaena rubida (Oligochaeta) in a base metal mining area. Environ. Pollut.10, 201–208 (1976)

  34. Ireland, M.P., Wootton, R.J.: Distribution of lead, zinc, copper and manganese in the marine gastropodsThais lapillus andLittorina littorea, around the coasts of Wales. Environ. Pollut.12, 27–41 (1977)

  35. Kahn, H.L.: A background correction system for atomic absorption. At. Absorption Newslett.7, 40–43 (1968)

  36. Kendall, M.G., Stuart, A.: The Advanced Theory of Statistics, Vol. 2, Section 29.24. London: Griffin 1967

  37. Kinrade, J.D., Van Loon, J.C.: Solvent extraction for use with flame atomic absorption spectrometry. Analyt. Chem.46, 1894–1898 (1974)

  38. Lagerwerff, J.V., Specht, A.W.: Contamination of roadside soil and vegetation with cadmium, nickel, lead and zinc. Environ. Sci. Technol.4, 583–586 (1970)

  39. Manly, R., George, W.O.: The occurrence of some heavy metals in populations of the freshwater musselAnodonta anatina (L.) from the River Thames. Environ. Pollut.14, 139–154 (1977)

  40. Martin, M.H., Coughtrey, P.J.: Preliminary observations on the levels of cadmium in a contaminated environment. Chemosphere4, 155–160 (1975)

  41. Martin, M.H., Coughtrey, P.J.: Comparisons between the levels of lead, zinc and cadmium within a contaminated environment. Chemosphere5, 15–20 (1976)

  42. Martin, M.H., Coughtrey, P.J., Young, E.W.: Observations on the availability of lead, zinc, cadmium and copper in woodland litter and the uptake of lead, zinc and cadmium by the wood-louse,Oniscus asellus. Chemosphere5, 313–318 (1976)

  43. Maurer, R.: The beetle and spider fauna of meadows affected by traffic pollution. Oecologia (Berl.)14, 327–351 (1974)

  44. Mclean, R.O., Shields, B.: A study of the factors causing changes in the lead levels of crops growing beside roadways. Environ. Pollut.14, 267–273 (1977)

  45. Meincke, K.-F., Schaller, K.-H.: Use of the snailHelix pomatia (L.) on cultivated land as indicator of environmental pollution with iron, zinc, and lead. Oecologia (Berl.)15, 393–398 (1974)

  46. Morris, D.: The snail-eating behaviour of thrushes and blackbirds. Br. Birds47, 33–49 (1954)

  47. Neathery, M.W., Miller, W.J.: Metabolism and toxicity of cadmium, mercury, and lead in animals: a review. J. Dairy Sci.58, 1767–1781 (1975)

  48. Nordberg, G.F.: Cadmium metabolism and toxicity. Environ. Physiol. Biochem.2, 7–36 (1972)

  49. Olsson, M., Kihlström, J. E., Jensen, S., Örberg, J.: Cadmium and mercury concentrations in mink (Mustela vison) after exposure to PCBs. Ambio8, 25 (1979)

  50. Pequegnat, J.E., Fowler, S.W., Small, L.F.: Estimates of the zinc requirements of marine organisms. J. Fish. Res. Bd. Canada26, 145–150 (1969)

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

  52. Price, P., Rathcke, B.J., Gentry, D.A.: Lead in terrestrial arthropods: evidence for biological concentration. Environ. Entomol.3, 370–372 (1974)

  53. Pringle, B.H., Hissong, D.E., Katz, E.L., Mulawka, S.T.: Trace metal accumulation by estuarine molluscs. J. Sanit. Eng. Div.: Proc. Amer. Soc. Civ. Eng.94, 455–475 (1968)

  54. Ricker, W.E.: Linear regressions in fishery research. J. Fish. Res. Bd. Canada30, 409–434 (1973)

  55. Roberts, R.D., Johnson, M.S.: Dispersal of heavy metals from abandoned mine workings and their transference through terestrial food chains. Environ. Pollut.16, 293–310 (1978)

  56. Schulz-Baldes, M.: Lead uptake from sea water and food, and lead loss in the common musselMytilus edulis. Mar Biol.25, 177–193 (1974)

  57. Segar, D.A., Collins, J.D., Riley, J.P.: The distribution of the major and some minor elements in marine animals. Part II. Molluscs. J. mar. biol. Ass. U.K.51, 131–136 (1971)

  58. Shaikh, Z.A., Lucis, O.J.: Biological differences in cadmium and zinc turnover. Arch. Environ. Health24, 410–418 (1972)

  59. Sokal, R.R., Rohlf, F.J.: Biometry. San Francisco: Freeman 1969

  60. Sumner, A.T.: The cytology and histochemistry of the digestive gland cells ofHelix. Quart. J. micr. Sci.106, 173–192 (1965)

  61. Vallee, B.L., Wacker, W.E.C.: Metallo-proteins. In: The Proteins, Vol. 5 (H. Neurath, ed.) London: Academic Press 1970

  62. Watling, H.R., Watling, R.J.: Trace metals in oysters from the Knysna estuary. Mar. Pollut. Bull.7, 45–48 (1976)

  63. Welch, J.M., Pollard, E.: The exploitation ofHelix pomatia L. Biol. Converv.8, 155–160 (1975)

  64. Wieser, W., Dallinger, R., Busch, G.: The flow of copper through a terrestrial food chain. II. Factors influencing the copper content of isopods. Oecologia (Berl.)30, 265–272 (1977)

  65. Williamson, P.: Use of65Zn to determine the field metabolism of the snailCepaea nemoralis L. Ecology56, 1185–1192 (1975)

  66. Williamson, P.: Size-weight relationships and field growth rates of the landsnailCepaea nemoralis L. J. Anim. Ecol.45, 875–885 (1976)

  67. Williamson, P.: Age determination of juvenile and adultCepaea. J. moll. Stud.45, 52–60 (1979a)

  68. Williamson, P.: Opposite effects of age and weight on cadmium concentrations of a gastropod mollusc. Ambio8, 30–31 (1979b)

  69. Williamson, P.: Comparison of metal levels in invertebrate detritivores and their natural diets: concentration factors reassessed. Oecologia (Berl.) (1979c)

  70. Williamson, P., Cameron, R.A.D., Carter, M.A.: Population dynamics of the landsnailCepaea nemoralis L.: a six-year study. J. Anim. Ecol.46, 181–194 (1977)

  71. Williamson, P., Evans, P.R.: Lead: levels in roadside invertebrates and small mammals. Bull. Environ. Contam. Toxicol.8, 280–288 (1972)

  72. Williamson, P., Evans, P.R.: A preliminary study of the effects of high levels of inorganic lead on soil fauna. Pedobiologia13, 16–21 (1973)

  73. Willson, R.: Zinc: a radical approach to disease. New Scientist76, 558–560 (1977)

  74. Wolda, H.: Ecology of some experimental populations of the landsnailCepaea nemoralis (L.). I. Adult numbers and adult mortality. Neth. J. Zool.22, 428–455 (1972)

  75. Wolda, H., Kreulen, D.A.: Ecology of some experimental populations of the landsnailCepaea nemoralis (L.). II. Production and survival of eggs and juveniles. Neth. J. Zool.23, 168–188 (1973)

  76. Wolfe, D.A.: Zinc enzymes inCrassostrea virginica. J. Fish. Res. Bd. Canada27, 59–69 (1970)

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Williamson, P. Variables affecting body burdens of lead, zinc and cadmium in a roadside population of the snailCepaea hortensis Müller. Oecologia 44, 213–220 (1980).

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  • Zinc
  • Cadmium
  • Vapour Pressure
  • Multiple Regression Analysis
  • Vapour Pressure Deficit