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Intracellular inclusions in the nematode Tripyloides marinus from metal-enriched and cleaner estuaries in Cornwall, south-west England

Published online by Cambridge University Press:  11 May 2009

R. N. Millward
R. N. Millward
Affiliation:
School of Environmental Sciences, University of East Anglia, Norwich, NR4 7TY
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Extract

Two types of electron-dense inclusions are described using transmission electron microscopy from the marine nematode Tripyloides marinus (Nematoda; BÜtshli, 1874) isolated from a metal-enriched site and a site of low metal contamination. These were classified as granular, intracellular inclusions in the intestinal syncytium, and fluid-filled vesicles along the cuticular margin of the epidermis. Energy-dispersive x-ray analysis (EDX) showed that the intestinal granules were largely comprised of P and S, with variable levels of Ca, Cu, Zn, Fe and Br, and that the epidermal vesicles contained high levels of Br and S with variable levels of Ca, Cu, Zn, Fe and P. It is suggested that intestinal granule formation may be involved in the detoxification of heavy metal sulphides and might result in a heightened ability of the species to colonize metal-enriched sediments. The function of the cuticular vesicles is unclear, but might be linked to a predatory or microbial defence mechanism (Woodin et al., 1987), or as part of a metal detoxification system.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 76 , Issue 4 , November 1996 , pp. 885 - 895
Copyright
Copyright © Marine Biological Association of the United Kingdom 1996

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References

Ashida, J., Higashi, N. & Kikuchi, T., 1963. An electron microscopic study on copper precipitation by copper resistant yeast cells. Protoplasma, 57, 27–32.CrossRefGoogle Scholar
Bird, A.F. & Bird, J., 1971. The structure of nematodes. San Diego: Academic Press.Google Scholar
Brown, B.E., 1976. Observations on the tolerance of the isopod Asellus meridianus Rac. to copper and lead. Water Research, 10, 555–559.CrossRefGoogle Scholar
Brown, B.E., 1977. Uptake of copper and lead by a metal-tolerant isopod Asellus meridianus Rac. Freshwater Biology, 7, 235–244.CrossRefGoogle Scholar
Brown, B.E., 1982. The form and function of metal-containing ‘granules’ in invertebrate tissues. Biological Reviews, 57, 621–667.CrossRefGoogle Scholar
Bryan, G. W., 1974. Concentration of zinc and copper in the tissues of decapod crustaceans. Journal of the Marine Biological Association of the United Kingdom, 48, 303–321.CrossRefGoogle Scholar
Bryan, G.W. & Gibbs, P.E., 1983. Heavy metals in the Fal Estuary, Cornwall: a study of long-term contamination by mining waste and its effects on estuarine organisms. Occasional Publications; Marine Biological Association, no. 2,112 pp.Google Scholar
Bryan, G.W. & Hummerstone, L.G., 1971. Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of heavy metals. I. General observations and adaptation to copper. Journal of the Marine Biological Association of the United Kingdom, 51, 845–863.CrossRefGoogle Scholar
Bryan, G.W. & Hummerstone, L.G., 1973. Adaptation of the 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
Carbonell, L.M. & Apitz, R.J., 1959. Histochemical study of a pigment in the digestive tube of Ascaris lumbricoides. Experimental Parasitology, 8, 591–595.CrossRefGoogle ScholarPubMed
Chitwood, B.G. & Chitwood, M.B., 1938. Further notes on intestinal cell inclusions in nematodes. Proceedings of the Helminthological Society, Washington, DC, 5,16–18.Google Scholar
Chitwood, B.G. & Chitwood, M.B., 1950. An introduction to nematology. Baltimore: Monumental Printing.Google Scholar
Coombs, T.L. & George, S.G., 1978. Mechanisms of immobilization and detoxification of metals in marine organisms. In Physiology and behaviour of marine organisms. Proceedings of the 12th European Symposium on Marine Biology, Stirling, Scotland, 5–12 September, 1977 (ed. D.S., McLusky and A.J., Berry), pp. 179–187. Oxford: Pergamon Press.Google Scholar
George, S.G. & Pirie, B.J.S., 1979. The occurrence of cadmium in sub-cellular particles in the kidney of the marine mussel, Mytilus edulis, exposed to cadmium. The use of electron microprobe analysis. Biochimica et Biophysica Acta, 580, 234–244.CrossRefGoogle ScholarPubMed
George, S.G., Pirie, B.J.S., Cheyne, A.R., Coombs, T.L. & Grant, P.T., 1978. Detoxication of metals by marine bivalves: an ultrastructural study of the compartmentation of copper and zinc in the oyster Ostrea edulis. Marine Biology, 45,147–156.CrossRefGoogle Scholar
Grant, A. & Millward, R.N., 1994. The impact of a sudden increase in metal discharges to Restronguet Creek, Cornwall, UK: an estuary already severely contaminated with heavy metals. In Environmental contamination. Proceedings of the 6th International Conference (ed. S.P., Varnavas), pp. 272–274. Edinburgh: CEP Consultants Ltd.Google Scholar
Hateley, J.G., Grant, A. & Jones, N.V., 1989. Heavy metal tolerance in estuarine populations of Nereis diversicolor. In Reproduction, genetics and distributions of marine organisms. Proceedings of the 23rd European Symposium on Marine Biology, Swansea, Wales, 5–9 September, 1988 (ed. J.S., Ryland and P.A., Tyler), pp. 379–385. Fredensborg, Denmark: Olsen & Olsen.Google Scholar
Heip, C, Vincx, M. & Vranken, G., 1985. The ecology of marine nematodes. Oceanography and Marine Biology. Annual Review. London, 23, 399–489.Google Scholar
Icely, J.D. & Nott, J.A. 1980. Accumulation of copper within the ‘hepatopancreatic’ caeca of Corophium volutator (Crustacea: Amphipoda). Marine Biology, 57,193–199.CrossRefGoogle Scholar
Jacobs, L.J., 1987. A checklist of the Monhysteridae (Nematoda, Monhysterida). Johannesburg: Rand Afrikaans University.Google Scholar
Jeantet, A.Y., Ballan-Dufrancais, C. & Martin, J.L., 1985. Recherche des mecanismes de detoxication du cadmium par l'huitre Crassostrea gigas (Mollusc, Bivalve). II. Sites intracellulaires d'accumulation du metal dans les organes absorbants et excreteurs. Comptes Rendus de I'Academie de Sciences. Paris, serie III, 301(5), 177–182.Google Scholar
Juget, J., 1969. Lafaune benthique du Leman - modalites et determinisme ecologique du peuplement. PhD thesis, University of Lyon, France.Google Scholar
Lee, C.C., 1970. Ancylostoma caninum: fine structure of intestinal epithelium. Experimental Parasitology, 24, 336–347.CrossRefGoogle Scholar
Mason, A.Z. & Nott, J.A., 1981. The role of intracellular biomineralized granules in the regulation and detoxification of metals in gastropods with special reference to the marine prosobranch Littorina littorea. Aquatic Toxicology, 1, 239–256.CrossRefGoogle Scholar
Mason, A.Z., Simkiss, K. & Ryan, K.P., 1984. The ultrastructural localization of metals in speci-mens of Littorina littorea collected from clean and polluted sites. Journal of the Marine Biological Association of the United Kingdom, 64, 699–720.CrossRefGoogle Scholar
Millward, R.N. & Grant, A., 1995. Assessing the impact of copper on nematode communities from a chronically metal-enriched estuary using pollution induced community tolerance. Marine Pollution Bulletin, 30, 701–706.CrossRefGoogle Scholar
Nicholas, W.L., Goodchild, D.J. & Stewart, A., 1987. The mineral composition of intracellular inclusions in nematodes from thiobiotic mangrove mud-flats. Nematologica, 33, 167–179.CrossRefGoogle Scholar
Nott, J.A., Bebianno, M.J., Langston, W.J. & Ryan, K.P., 1993. Cadmium in the gastropod Littorina littorea. Journal of the Marine Biological Association of the United Kingdom, 73, 655–665.CrossRefGoogle Scholar
Nott, J.A. & Nicolaidou, A., 1989. The cytology of heavy metal accumulations in the digestive glands of three marine gastropods. Proceedings of the Royal Society of London B, 237, 347–362.Google Scholar
Nufi, B., 1984. Ultrastructurelle und okophysiologische Untersuchungen an kristalloiden Einschliissen der Muskeln eines sulfidtoleranten limnischen Nematoden (Tobrilus gracilis). Verb'ffentlichungen Institutsfiir Meeresforschung in Bremerhaven, 20, 3–15.Google Scholar
Nufi, B. & Trimkowski, V., 1984. Physikalische Mikroanalysen an kristalloiden Einschliissen bei Tobrihis gracilis (Nematoda, Enoplida). Veroffentlichungen Instituts fiir Meeresforschung in Bremerhaven, 20,17–27.Google Scholar
Reimann, F., 1970. Freilebende Nematoden aus der Grenzbereich Meer-Siifi-Wasser in Kolumbien, Sudamerika. Veröffentlichungen Instituts fÜr Meeresforschung in Bremerhaven, 12, 365–412.Google Scholar
Simkiss, K., 1981. Calcium, pyrophosphate and cellular pollution. Trends in Biochemical Science, 6(4), 3–5.Google Scholar
Simkiss, K., Taylor, M. & Mason, A.Z., 1982. Metal detoxification and bioaccumulation in molluscs. Marine Biology Letters, 3,187–201.Google Scholar
Somerfield, P.J., Gee, J.M. & Warwick, R.M., 1994. Soft sediment meiofaunal community structure in relation to a long-term heavy metal gradient in the Fal estuary system. Marine Ecology Progress Series, 105, 79–88.CrossRefGoogle Scholar
Tietjen, J.H., 1980. Population structure and species composition of the free-living nematodes inhabiting sands of the New York Bight Apex. Estuarine and Coastal Marine Science, 10, 61–73.CrossRefGoogle Scholar
Waku, Y. & Sumimoto, K., 1974. Metamorphosis of midgut epithelial cells in the silkworm (Bombyx mori) with special regard to the calcium salt deposits in the cytoplasm. II. Electron microscopy. Tissue and Cell, 6,127–136.CrossRefGoogle Scholar
Walker, G., 1977. ‘Copper’ granules in the barnacle Balanus balanoides. Marine Biology, 39,343–349.CrossRefGoogle Scholar
Walker, G., Rainbow, P.S., Foster, P. & Holland, D.L., 1975. Zinc phosphate granules in tissue surrounding the midgut of the barnacle Balanus balanoides. Marine Biology, 33,161–166.CrossRefGoogle Scholar
Woodin, S.A., Walla, M.D. & Lincoln, D.E., 1987. Occurrence of brominated compounds in soft-bottom benthic organisms. Journal of Experimental Marine Biology and Ecology, 107, 209–217.CrossRefGoogle Scholar