Skip to main content
SpringerLink
Log in

Trace-metal detoxification and tolerance of the estuarine worm Hediste diversicolor chronically exposed in their environment

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Polychaete worms (Hediste diversicolor) originating from a strongly metal-contaminated area (Restronguet Creek) and a relatively clean site (Blackwater estuary) were exposed to a range of experimental doses of Ag, Cd, Cu and Zn. Specimens from both populations were compared to assess their relative sensitivity to metal stress and the physiological mechanisms involved in their respective adaptive strategies for coping with increased metal exposures. Taking into account the LC50 values, increased tolerance to Cd, Cu and Zn of the Restronguet Creek worms over that of the Blackwater was demonstrated, whereas the opposite was shown for Ag. An abundant secretion of mucus in response to toxicants was observed, possibly reducing metal availability for uptake, at least under laboratory conditions. This mechanism was particularly active in specimens from Restronguet Creek exposed to Ag and Cu. Unexpectedly, of the two worm populations, Blackwater worms contained significantly higher concentrations of cytosolic heat-stable compounds (CHSTC), a category of cytosolic components that includes metallothioneins, the detoxificatory role of which is well documented, and other compounds binding trace metals via sulphur bonds. However, the concentration of such compounds is not totally representative in itself of their involvement in metal detoxification, because a high rate of their turnover in metal-exposed worms might be responsible for (at least) the Cu storage associated with S in lysosomes as a consequence of the breakdown of Cu-thionein. Cu-containing lysosomes were abundant in epidermal cells of Restronguet Creek worms, but were lacking in Blackwater worms. Extracellular granules present in the epicuticle also contained S and Cu, their number and size being much more important in Restronguet Creek worms, and they appear to be a major detoxificatory store for accumulated Cu. Spherocrystals in cells of the gut wall seem to be the major detoxified store of Zn in Restronguet Creek worms, whereas in specimens from the Blackwater they were also present but contained only S and Ca at detectable levels. Evidence was also found for the presence of detoxificatory intracellular structures containing other metals and metalloids in the tegument and gut epithelium of Restronguet Creek worms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2a, b.
Fig. 3.
Fig. 4a–d.
Fig. 5a–e.
Fig. 6a–c.
Fig. 7a, b.
Fig. 8a, b.

Similar content being viewed by others

References

  • Amiard JC, Pineau A, Boiteau HL, Métayer C, Amiard-Triquet C (1987) Application of atomic absorption spectrophotometry using Zeeman effect to the determination of eight trace elements (Ag, Cd, Cr, Cu, Mn, Ni, PB and Se) in biological materials. Water Res 21:693–697

    CAS  Google Scholar 

  • Berthet B, Mouneyrac C, Amiard JC, Amiard-Triquet C, Berthelot Y, Rainbow PS, Smith BD (2003) Response to metals of the polychaete annelid Hediste diversicolor, a key species in estuarine and coastal sediments. Arch Environ Contam Toxicol (in press)

  • Bliss CI (1938) The determination of the dosage–mortality curve from small numbers. Q J Pharmacol 2:192–216

    Google Scholar 

  • Boilly B, Richards A (1978) Accumulation de fer chez une annélide polychète: Magelona papillicornis (M). CR Acad Sci Paris 286:1005–1008

    CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brdicka A (1933) Polarographic studies with the dropping mercury method. A new test for proteins in the presence of cobalt salts in ammoniacal solution of ammonium chloride. Collect Czech Chem Commun 5:112–128

    CAS  Google Scholar 

  • Brown BE (1982) The form and function of metal-containing "granules" in invertebrate tissues. Biol Rev 57:621–667

    CAS  Google Scholar 

  • Bryan GW (1974) Adaptation of an estuarine polychaete to sediments containing high concentrations of heavy metals. In: Vernberg FJ, Vernberg WB (eds) Pollution and physiology of marine organisms. Academic, New York, pp 123–135

  • Bryan GW (1976) Some aspects of heavy metal tolerance in aquatic organisms. In: Lockwood APM (ed) Effects of pollutants on aquatic organisms. Cambridge University Press, Cambridge, pp 7–34

  • Bryan GW, Gibbs PE (1983) Heavy metals in the Fal Estuary, Cornwall: a study of long-term contamination by mining waste and its effects on estuarine organisms. Occas Publ Mar Biol Assoc UK 2:1–112

    Google Scholar 

  • Bryan GW, Hummerstone LG (1971) Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of heavy metals. I. General observations and adaptation to copper. J Mar Biol Assoc UK 51:845–863

    CAS  Google Scholar 

  • Bryan GW, Hummerstone LG (1973) Adaptation of the polychaete Nereis diversicolor to estuarine sediments containing high concentrations of zinc and cadmium. J Mar Biol Assoc UK 53:839–857

    CAS  Google Scholar 

  • Bryan GW, Langston WJ, Hummerstone, Burt GR (1985) A guide to the assessment of heavy metal contamination in estuaries using biological indicators. Occas Publ Mar Biol Assoc UK 4:1–9

    Google Scholar 

  • Bryan GW, Gibbs PE, Hummerstone LG, Burt GR (1987) Copper, zinc, and organotin as long-term factors governing the distribution of organisms in the Fal Estuary in Southwest England. Estuaries 10:208–219

    CAS  Google Scholar 

  • Campbell MJ, Radecki Z, Trinkl A, Burns KI (2000) Report on the intercomparison runs for the determination of trace and minor elements in cabbage material. Rep. IAEA/AL/123, IAEA-359, Vienna

  • Coquery M, Horvat M (1996) The analytical performance study for the MED POL area: determination of trace-elements in marine sediment SD-MEDPOL-1/TM and fish homogenate MA-MEDPOL-1/TM. Report, IAEA, Monaco

    Google Scholar 

  • Couillard Y, Campbell PGC, Tessier A, Pellerin-Massicotte J, Auclair JC (1995) Field transplantation of a freshwater bivalve, Pyganodon grandis, across a metal contamination gradient. I. Temporal changes in metallothionein and metal (Cd, Cu and Zn) concentrations in soft tissues. Can J Fish Aquat Sci 52:690–702

    CAS  Google Scholar 

  • Dennaï N, Dhainaut-Courtois N, Bouquegneau JM, Nejmeddine A (1986) Effets du cadmium et du mercure sur un ver marin (Nereis diversicolor O.F. Müller). Mécanismes de détoxication. CR Acad Sci Paris 302:489–494

    Google Scholar 

  • Dines HG (1969) The metalliferous mining region of south-west England. Her Majesty's Stationery Office, London

  • Farmanfarmaian A (1985) Fractional distribution of 203HgCl2 and CH3 203HgCl in the intestine of a marine fish. Mar Environ Res 17:176–180

    CAS  Google Scholar 

  • Fernandez TV, Jones NV (1989) The distribution of zinc in the body of Nereis diversicolor. Trop Ecol 30:285–293

    Google Scholar 

  • Gabe M (1968) Techniques histologiques. Masson and Cie, Paris

  • George SG (1982) Subcellular accumulation and detoxication of metals in aquatic animals. In: Vernberg WB, Calabrese A, Thurberg F, Vernberg FJ (eds) Physiological mechanisms of marine pollutants' toxicity. Academic, New York, pp 3–55

  • Gibbs PE, Burt GR, Pascoe PL, Llewellyn CA, Ryan KP (2000) Zinc, copper and chlorophyll-derivatives in the polychaete Owenia fusiformis. J Mar Biol Assoc UK 80:235–248

    Article  CAS  Google Scholar 

  • Grant A, Hateley JG, Jones NV (1989) Mapping the ecological impact of heavy metals in the estuarine polychaete Nereis diversicolor using inherited metal tolerance. Mar Pollut Bull 20:235–238

    CAS  Google Scholar 

  • Hateley JG, Grant A, Jones NV (1989) Heavy metal tolerance in estuarine populations of Nereis diversicolor. In: Ryland JS, Tyler PA (eds) Reproduction, genetics and distribution of marine organisms. Proc 23rd Eur Mar Biol Symp. Olsen and Olsen, Fredensborg, pp 379–385

  • Hummel H, Paternello T (1994) Genetic effects of pollutants on marine and estuarine invertebrates. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapman and Hall, London, pp 425–434

  • Hummel H, Amiard-Triquet C, Bachelet G, Desprez M, Marchand J, Sylvand B, Amiard JC, Rybarczyk H, Bogaards RH, Sinke J, de Wit Y, de Wolf L (1996) Sensitivity to stress of the estuarine bivalve Macoma balthica from areas between the Netherlands and its southern limits (Gironde). J Sea Res 35:315–321

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Klerks PL, Weis JS (1987) Genetic adaptation to heavy metals in aquatic organisms: a review. Environ Pollut 45:173–205

    CAS  Google Scholar 

  • Koechlin N, Grasset M (1988) Silver contamination in the marine polychaete annelid Sabella pavonina. a cytological and analytical study. Mar Environ Res 26:249–263

    CAS  Google Scholar 

  • Langston WJ (1980) Arsenic in UK estuarine sediments and its availability to benthic organisms. J Mar Biol Assoc UK 60:869–881

    Google Scholar 

  • Langston WJ, Bebianno MJ, Burt GR (1998) Metal handling strategies in molluscs. In: Langston WJ, Bebianno MJ (eds) Metal metabolism in aquatic environment. Chapman and Hall, London, pp 219–283

  • Luoma SN (1977) Detection of trace contaminant effects in aquatic ecosystems. J Fish Res Board Can 34:436–443

    Google Scholar 

  • Marigomez I, Soto M, Cajaraville MP (1995) Morphofunctional patterns of cell and tissue systems involved in metal handling and metabolism. In: Cajaraville MP (ed) Cell biology in environmental toxicology. University of the Basque Country Press, Bilbao, Spain, pp 89–134

  • Mason AZ, Jenkins KD (1995) Metal detoxification in aquatic organisms. In: Tessier A, Turner DR (eds) Metal speciation and bioavailability in aquatic systems. Wiley, Chichester, pp 479–608

  • Morgan JE, Morgan AJ (1989) Zinc sequestration by earthworms (Annelida, Oligochaeta) chloragocytes. An in vivo investigation using fully quantitative electron probe X-ray micro-analysis. Histochemistry 90:405–411

    CAS  PubMed  Google Scholar 

  • Mouneyrac C, Amiard JC, Amiard-Triquet C, Cottier A, Rainbow PS, Smith BD (2002) Partitioning of accumulated trace metals in the talitrid amphipod crustacean Orchestia gammarellus: a cautionary tale on the use of metallothionein-like proteins as biomarkers. Aquat Toxicol 57:225–242

    Article  CAS  PubMed  Google Scholar 

  • Nassiri Y, Rainbow PS, Amiard-Triquet C, Rainglet F, Smith BD (2000) Trace metal detoxification in the ventral caeca of Orchestia gammarellus (Crustacea: Amphipoda). Mar Biol 136:477–484

    Article  CAS  Google Scholar 

  • Noël-Lambot F (1981) Presence in the intestinal lumen of marine fish of corpuscles with a high cadmium-, zinc- and copper-binding capacity: a possible mechanism of heavy metal tolerance. Mar Ecol Prog Ser 4:175–181

    Google Scholar 

  • Pirie B, Fayi L, George SG (1985) Ultrastructural localisation of copper and zinc in the polychaete Nereis diversicolor, from a highly contamined estuary. Mar Environ Res 17:197–198

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Rainbow PS (1995) Physiology, physicochemistry and metal uptake—a crustacean perspective. Mar Pollut Bull 31:55–59

    Article  CAS  Google Scholar 

  • Rainbow PS (1997) Ecophysiology of trace metal uptake in crustaceans. Estuar Coast Shelf Sci 44:169–175

    Article  CAS  Google Scholar 

  • Rainbow PS, Amiard-Triquet C, Amiard JC, Smith BD, Best SL, Nassiri Y, Langston W (1999) Trace metal uptake rates in crustaceans (amphipods and crabs) from coastal sites in NW Europe differentially enriched with trace metals. Mar Ecol Prog Ser 183:189–203

    CAS  Google Scholar 

  • Thompson JAJ, Cosson RP (1984) An improved electrochemical method for the quantification of metallothionein in marine organisms. Mar Environ Res 11:137–152

    CAS  Google Scholar 

  • Thompson M, Wood R (1993) The international harmonized protocol for the proficiency testing of chemical analytical laboratories. IUPAC/ISO/AOAC. J Pure Appl Chem 65:2123–2144

    CAS  Google Scholar 

  • Viarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Physiol C 104:355–372

    Article  Google Scholar 

  • Vovelle J, Grasset M (1991) Experimental silver bioaccumulation in the polychaete Pomatoceros triqueter. Biometals 4:107–112

    CAS  Google Scholar 

  • Wallace WG, Lopez GR, Levinton JS (1998) Cadmium resistance in an oligochaete and its effects on cadmium trophic transfer to an omnivorous shrimp. Mar Ecol Prog Ser 172:225–237

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank A. Anglo and L. Massot for their technical help in preparing the samples for EPMA and electron microscopy. Studies were carried out at the Centre de microscopie électronique de l'IFR de Biologie Intégrative and the Service inter-universitaire Assistance à la Recherche, Université Pierre et Marie Curie, Paris, France. This work was carried out in the framework of a PICS (International Programme of Scientific Co-operation) project funded by the CNRS (French National Scientific Research Centre). All the experiments presented in this paper complied with the current laws of the United Kingdom, where they were performed.

Author information

Authors and Affiliations

  1. CEREA, Université Catholique de l'Ouest, 3 Place A. Leroy, BP 808, 49008, Angers, France

    C. Mouneyrac & O. Mastain

  2. CNRS-GDR 1117, ISOMer, SMAB, 2 Rue de la Houssinière, BP 92208, 44322, Nantes Cedex 3, France

    C. Mouneyrac, O. Mastain, J. C. Amiard & C. Amiard-Triquet

  3. Service de Microscopie électronique et Cytophysiologie analytique, Université Pierre et Marie Curie, 8 et 12 Rue Cuvier, 75252, Paris Cedex 5, France

    P. Beaunier & A.-Y. Jeantet

  4. Department of Zoology, The Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    B. D. Smith & P. S. Rainbow

Authors
  1. C. Mouneyrac
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. O. Mastain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. C. Amiard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Amiard-Triquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Beaunier
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A.-Y. Jeantet
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. B. D. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. P. S. Rainbow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Mouneyrac.

Additional information

Communicated by S.A. Poulet, Roscoff

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mouneyrac, C., Mastain, O., Amiard, J.C. et al. Trace-metal detoxification and tolerance of the estuarine worm Hediste diversicolor chronically exposed in their environment. Marine Biology 143, 731–744 (2003). https://doi.org/10.1007/s00227-003-1124-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-003-1124-6

Keywords

Search

Navigation