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The accumulation and intracellular compartmentation of cadmium, lead, zinc and calcium in two earthworm species (Dendrobaena rubida and Lumbricus rubellus) living in highly contaminated soil

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Summary

The earthworm Lumbricus rubellus contained more Ca and Zn, and less Pb and Cd, than Dendrobaena rubida living in the same contaminated disused-mine soil. Differences in the kinetics of Ca turnover may account for some of the inter-specific differences in heavy metal burdens, although the calciferous glands do not seem to be directly involved in heavy metal excretion. A comparison of the present findings with published data indicated that the concentration of soil Ca and the bioavailability of heavy metals, both factors being allied to soil pH, are important exogenous determinants of heavy metal accumulation by different earthworm populations. Electron microprobe X-ray analysis of air-dried smears of chloragogenous tissue showed that the metals were fairly specifically compartmentalized into two distinct organelles in both worms: Ca, Pb and Zn were found (associated with P) in the chloragosomes; Cd was found (with S and probably in stoichiometric association) in a more electron-lucent vesicular component, designated the ‘cadmosome’, but which may be identical with the debris vesicles which are characteristic inclusions in conventionally-fixed chloragocytes. The in vivo incorporation of Pb by the chloragosomes of D. rubida was accompanied by the loss of Ca, Zn and P.

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References

  • Appleton TC (1978) The contribution of cryoultramicrotomy to X-ray microanalysis in biology. In: Erasmus DA (ed) Electron probe microanalysis in biology. Chapman and Hall, London, pp 148–182

    Google Scholar 

  • Ash CPJ, Lee DL (1980) Lead, cadmium, copper and iron in earthworms from roadside sites. Environ Pollut 22:59–67

    Google Scholar 

  • Chandler JA, Battersby S (1976) X-ray microanalysis of ultrathin frozen and freeze dried sections of human sperm cells. J Microsc 107:55–65

    Google Scholar 

  • Cooke M, Jackson A, Nickless G, Roberts DJ (1979) Distribution and speciation of cadmium in the terrestrial snail, Helix aspersa. Bull Environ Contam Toxicol 23:445–451

    Google Scholar 

  • Coombs TL, George SG (1977) Mechanisms of immobilization and detoxication of metals in marine organisms. In: Mclusky DS, Berry AJ (eds) Physiology and behaviour of marine organisms. Pergamon Press, Oxford, pp 179–187

    Google Scholar 

  • Davies BE (1980) Trace element pollution. In: Davies BE (ed) Applied soil trace elements. John Wiley and Sons, Chichester, New York, Brisbane, Toronto, pp 287–351

    Google Scholar 

  • Fischer E, Trombitas K (1980) X-ray microprobe analysis of chloragosomes of untreated and of EDTA-treated Lumbricus terrestris by using fresh air-dried smears. Acta Histochem 66:237–242

    Google Scholar 

  • Foster P (1976) Concentration and concentration factors of heavy metals in brown algae. Environ Pollut 10:45–54

    Google Scholar 

  • George SG, Nott JA, Pirie BJS, Mason AZ (1976) A comparative quantitative study of cadmium retention in tissues of a marine bivalve during different fixation and embedding procedures. Proc R Microsc Soc II (Micro'76 Suppl), p 42

    Google Scholar 

  • George SG, Pirie BJS, Cheyne AR, Coombs TL, Grant PT (1978) Detoxication of metals by marine bivalves: an ultrastructural study of the compartmentation of copper and zinc in the oyster Ostrea edulis. Mar Biol 45:147–156

    Google Scholar 

  • George SG, Pirie BJS (1979) The occurrence of cadmium in subcellular particles, in the kidney of the marine mussel, Mytilus edulis, exposed to cadmium. Biochim Biophys Acta 580:234–244

    Google Scholar 

  • George SG, Carpene E, Coombs TL, Overnell J, Youngson A (1979) Characterization of cadmium-binding proteins from mussels, Mytilus edulis (L), exposed to cadmium. Biochim Biophys Acta 580:225–233

    Google Scholar 

  • Gish CD, Christensen RE (1973) Cadmium, nickel, lead and zinc in earthworms from roadside soil. Environ Sci Technol 7:1060–1062

    Google Scholar 

  • Gullvag BM (1978) Metal measured in earthworm tissue by X-ray microanalysis. In: Sturgess JM (ed) Electron microscopy 1978, Vol. 2: Biology. Microscopical Society of Canada, Toronto, pp 114–115

    Google Scholar 

  • Howard AG, Nickless G (1975) Protein binding of cadmium, zinc and copper in environmentally insulated limpets, Patella vulgata. J Chromat 104:457–459

    Google Scholar 

  • Howard AG, Nickless G (1977) Heavy metal complexation in polluted molluscs. I. Limpets (Patella vulgata and Patella intermedia). Chem Biol Interact 16:107–114

    Google Scholar 

  • Hsu FS, Krook L, Pond WG, Duncan JR (1975) Interactions of dietary calcium with toxic levels of lead and zinc in pigs. J Nutr 105:112–118

    Google Scholar 

  • Icely JD, Nott JA (1980) Accumulation of copper within the hepatopancreatic caeca of Corophium volutator (Crustacea: Amphipoda). Mar Biol 57:193–199

    Google Scholar 

  • Ireland MP (1975a) Metal content of Dendrobaena rubida (Oligochaeta) in a base metal mining area. Oikos 26:74–79

    Google Scholar 

  • Ireland MP (1975b) Distribution of lead, zinc and calcium in Dendrobaena rubida (Oligochaeta) living in soil contaminated by base metal mining in Wales. Comp Biochem Physiol 52 B:551–555

    Google Scholar 

  • Ireland MP (1978) Heavy metal binding properties of earthworm chloragosomes. Acta Biol Hung 29:385–394

    Google Scholar 

  • Ireland MP (1979) Metal accumulation by the earthworms Lumbricus rubellus, Dendrobaena veneta and Eiseniella tetraedra living in heavy metal polluted sites. Environ Pollut 19:201–206

    Google Scholar 

  • Ireland MP (1981a) Uptake and distribution of cadmium in the slug Arion ater (L.). Comp Biochem Physiol 68 A:37–41

    Google Scholar 

  • Ireland MP (1981 b) Earthworms and heavy metals. In: The Proceedings of the Darwin Centenary Symposium on Earthworm Ecology, Sept. 1981. Pedobiologia (In press)

  • Ireland MP, Richards KS (1977) The occurrence and localization of heavy metals and glycogen in the earthworms Lumbricus rubellus and Dendrobaena rubida from a heavy metal site. Histochemistry 51:153–166

    Google Scholar 

  • Ireland MP, Richards KS (1981) Metal content, after exposure to cadmium, of two species of earthworms of known differing calcium metabolic activity. Environ Pollut 26:69–78

    Google Scholar 

  • Ireland MP, Wooton RJ (1976) Variations in the lead, zinc and calcium content of Dendrobaena rubida (Oligochaeta) in a base metal mining area. Environ Pollut 10:201–208

    Google Scholar 

  • Jarvis SC, Jones LHP, Hopper MJ (1976) Cadmium uptake from solution by plants and its transport from roots to shoots. Plant Soil 44:179–191

    Google Scholar 

  • John MK (1976) Inter-relationships between plant cadmium and uptake of some other elements from culture solutions by oats and lettuce. Environ Pollut 11:85–95

    Google Scholar 

  • Kojima Y, Kagi JHR (1978) Metallothionein. Trends Biochem Sci 3:90–93

    Google Scholar 

  • Korte NE, Skopp J, Fuller WH, Niebla EE, Alesii BA (1976) Trace element movement in soils: influence of soil physical and chemical properties. Soil Sci 122:350–359

    Google Scholar 

  • Martin MH, Coughtrey PJ (1975) Preliminary observations on the levels of cadmium in a contaminated environment. Chemosphere 3:155–160

    Google Scholar 

  • Martin MH, Coughtrey PJ (1976) Comparisons between the levels of lead and cadmium within a contaminated environment. Chemosphere 5:15–20

    Google Scholar 

  • Morgan AJ (1979) Non-freezing techniques for preparing biological specimens for electron microprobe X-ray microanalysis. In: Johari O (ed) Scanning electron microscopy 1979, Vol. 2, SEM Inc., AMF O'Hare, Illinois, pp 635–648

    Google Scholar 

  • Morgan AJ (1980) Preparation of specimens. Changes in chemical integrity. In: Hayat MA (ed) X-ray microanalysis in biology. University Park Press, Baltimore, pp 65–165

    Google Scholar 

  • Morgan AJ (1981) A morphological and electron microprobe study of the inorganic composition of the mineralized secretory products of the calciferous gland and chloragogenous tissue of the earthworm, Lumbricus terrestris L. The distribution of injected strontium. Cell Tissue Res 220:829–844

    Google Scholar 

  • Morgan AJ, Davies TW, Erasmus DA (1978) Specimen preparation. In: Erasmus DA (ed) Electron probe microanalysis in biology. Chapman and Hall, London, pp 94–147

    Google Scholar 

  • Morgan AJ, Winters C (1982) The elemental composition of the chloragosomes of two earth-worm species (Lumbricus terrestris and Allolobophora longa) determined by electron probe X-ray microanalysis of freeze-dried cryosections. Histochemistry 73:589–598

    Google Scholar 

  • Noel-Lambot F (1976) Distribution of cadmium, zinc and copper in the mussel, Mytilus edulis. Existence of cadmium binding proteins similar to metallothioneins. Experientia 32:324–326

    Google Scholar 

  • Olafson RW, Sim RG, Kearns A (1979) Physiological and chemical characterization of invertebrate metallotheionein-like porteins. In: Kagi JHR, Nordberg M (eds) Metallotheionein, Birkhäuser Verlag, Basel, Boston, Stuttgart, pp 197–204

    Google Scholar 

  • Piearce TF (1972) The calcium relations of selected Lumbricidae. J Anim Ecol 41:167–188

    Google Scholar 

  • Prentø P (1979) Metals and phosphate in the chloragosomes of Lumbricus terrestris and their possible physiological significance. Cell Tissue Res 196:123–134

    Google Scholar 

  • Probst GS (1979) Cadmium: absorption, distribution and excretion in mammals. In: Mennear JH (ed) Cadmium toxicity. Marcel Dekker, New York Basel, pp 29–59

    Google Scholar 

  • Simkiss K (1976) Intracellular and extracellular routes of biomineralization. In: Calcium in biological systems, SEB Symposia No. 30. Cambridge University Press, Cambridge, pp 423–444

    Google Scholar 

  • Singhal RL, Merali Z (1979) Biochemical toxicity of cadmium. In: Mennear JH (ed) Cadmium toxicity. Marcel Dekker, New York Basel pp 61–112

    Google Scholar 

  • Suzuki KT, Takenaka S, Kubota K (1979) Fate and comparative toxicity of metallothioneins with differing Cd/Zn ratios in rat kidney. Arch Environ Contam Toxicol 8:85–95

    Google Scholar 

  • Tuck NW, Tuck JP (1971) Roman mine, Draethen, Glamorganshire. Bristol Exploration Club, Caving Report No, 15

  • Van Hook RI (1974) Cadmium, lead and zinc distribution between earthworms and soils. Potential for biological accumulation. Bull Environ Contam Toxicol 12:509–513

    Google Scholar 

  • Walker G (1977) “Copper” granules in the barnacle Balanus balanoides. Mar Biol 39:343–349

    Google Scholar 

  • Weser U, Rupp H (1979) Copper-thionein and other metal — sulphur — proteins. In: Kagi JHR, Nordberg M (eds) Metallothionein. Birkhäuser Verlag, Basel Boston Stuttgart pp 221–230

    Google Scholar 

  • Wielgus-Serafinska E, Kawka E (1976) Accumulation and localization of lead in Eisenia foetida (Oligochaeta) tissue. Folia Histochem Cytochem 14:315–320

    Google Scholar 

  • Williams AF (1981) Metal metabolism in earthworms. Unpublished M.Sc. thesis, University of Wales

  • Wright MA, Stringer A (1980) Lead, zinc and cadmium content of earthworms from pasture in the vicinity of an industrial smelting complex. Environ Pollut 23:313–321

    Google Scholar 

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Morgan, A.J., Morris, B. The accumulation and intracellular compartmentation of cadmium, lead, zinc and calcium in two earthworm species (Dendrobaena rubida and Lumbricus rubellus) living in highly contaminated soil. Histochemistry 75, 269–285 (1982). https://doi.org/10.1007/BF00496017

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