Abstract
Important Cd contamination has been observed in the Gironde estuary, France, but other metallic and organic pollutants are also present. Since sediment is well-known as a major compartment for the storage of numerous pollutants in aquatic environments, its contribution as a source of pollutants for the biota has been examined according to different methodologies. Geochemical studies have provided estimates of Cd mobility particularly with decreasing pHs and increasing salinity, a result in agreement with the relative abundance of exchangeable Cd and Cd bound to carbonates shown by sequential extraction. When in vitro assays tended to be more realistic with regard to the digestion process in bivalves, Cd extraction at low pH was lowered but was still important compared to Cu or Zn. Moreover, toxicity of Gironde sediments to copepod and sea urchin larval stages (not to oyster larvae) brought indirect evidence of the bioavailability of sediment-bound pollutants. Except the aromatic compound perylene, bioaccumulation in bivalves concerns mainly metals. In oysters they were found preferentially in the soluble phase and, in the cytosol, a strong relationship between cadmium and metallothionein-like proteins has been shown, suggesting a detoxication process in this species. This hypothesis is in agreement with the fact that neither cytopathological effects in gills and digestive glands nor marked changes of condition index were observed. On the other hand, no changes in MTLP levels in mussels were induced by metal accumulation in individuals transplanted from a comparatively unpolluted area (Bay of Bourgneuf). The stability of GST activity may be related to a poor accumulation of aromatic compounds. Changes in MDA concentration, AChE and catalase activities are discussed. Mobility, bioavailability of pollutants, significant responses of biomarkers suggest a potential environmental hazard. However, since interspecific differences occur, is the risk at the level of the whole estuarine ecosystem equilibrium or is it limited to a small number of species?
Similar content being viewed by others
References
Allen, H. E., R. H. Hall & T. D. Brisbin, 1980. Metal speciation: effects on aquatic toxicity. Envir. Sci. Technol. 14: 441–447.
Amiard, J. C., 1992. Bioavailability of sediment-bound metals for benthic aquatic organisms. In J. P. Vernet (eds), Impact of Heavy Metals on the Environment, Elsevier, Amsterdam: 183–202.
Amiard, J. C., A. Pineau, H. L. Boiteau, C. Métayer & C. Amiard-Triquet, 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. Wat. Res. 21: 693–697.
Amiard, J. C., H. Ettajani, A. Y. Jeantet, C. Ballan-Dufrançais & C. Amiard-Triquet, 1995. Bioavailability and toxicity of sediment-bound lead to a filter-feeder bivalve Crassostrea gigas (Thunberg). BioMetals 8: 280–289.
Baumard, P., H. Budzinski & P. Garrigues, 1997. Analytical procedure for the analysis of PAHs in biological tissues by gas chromatography coupled to mass spectrometry: application to mussels. Fresenius J. Anal. Chem. (in press).
Behar, F., C. Leblond & C. Saint Paul, 1989. Analyse quantitative des effluents de pyrolyse en milieu ouvert et fermé. Rev. Inst. Français Pét. 44: 387–411.
Beiras, R. & E. His, 1995. Toxicity of freeze-dried hydrocarbon polluted sediments to Crassostrea gigas embryos. Mar. Pollut. Bull. 30: 47–49.
Bocquené, G. & F. Galgani, 1991. L'acétylcholinestérase chez les organismes marins, outils de surveillance des effets des pesticides organophosphorés et carbamates. Oceanis 17: 439–448.
Boucaud-Camou, E., C. Lebesnerais, P. Lubet & I. Lihrmann, 1983. Dynamique et enzymologie de la digestion chez l'huître Crassostrea gigas (Thunberg). In IFREMER (ed.), Bases biologiques de l'Aquaculture. Montpellier, Actes de Colloques 1: 75–96.
Boutier, B., J. F. Chiffoleau, J. M. Jouanneau, C. Latouche & I. Philipps, 1989. La contamination de la Gironde par le cadmium: origine, extension, importance. IFREMER, Rapp. Sci. Tech. 14, 105 pp.
Budzinski, H., A. Papineau, P. Baumard & P. Garrigues, 1995. Extraction assistée par chauffage micro-ondes focalisées (MOF) à pression ambiante des composés organiques dans les matrices naturelles: application à l'analyse des composés aromatiques. C.R. Acad. Sci. Paris, 321 (Série IIb): 69–76.
Buege, J. A. & S. D. Aust, 1978. Microsomal lipid peroxydation. Meth. Enzymol. 50: 302–310.
Campbell, P. G. C., A. G. Lewis, P. M. Chapman, A. A. Crowder, W.K. Fletcher, B. Imber, S. N. Luoma, P. M. Stokes & M. Winfrey, 1988. Biologically available metals in sediments. Public. NRCC, Ottawa (Canada) Pub. N° NRCC 27694, 298 pp.
Carpene, E., 1993. Metallothionein in marine molluscs. In R. Dallinger & P. S. Rainbow (eds), Ecotoxicology of Metals in Invertebrates. Lewis Publishers, Boca Raton: 55–72.
Charlou, J. L. & M. Joanny, 1983. Dosage du mercure et d'autres métaux (Pb, Zn, Cu, Cd, Co, Ni, Cr, Mn) dans les sédiments marins par absorption atomique. In A. Aminot & M. Chaussepied (eds), Manuel des Analyses Chimiques en Milieu Marin, CNEXO, Brest: 285–295.
Claiborne, A., 1985. Catalase activity. In R. A. Greenwald (ed.), Handbook for Oxygen Radical Research, C.R.C. Press, Boca Raton, Florida: 283–284.
Coquery, M. & M. Horvat, 1996. The analytical performance study for the MED POL Area: determination of trace elements in marine sediment SD-MEDPOL-1/TM and in fish homogenate MA-MEDPOL-1/TM. In: International Atomic Energy Agency Marine Environment Laboratory, Monaco.
Cosson, R. P., C. Amiard-Triquet & J. C. Amiard, 1991. Metallothioneins and detoxification. Is the use of detoxication protein for MTs a language abuse? Wat. Air Soil Pollut. 57–58: 555–567.
Crouzet, C. & S. Altmann, 1996. Comparaison de diverses méthodologies pour estimer le pouvoir toxique de sédiments. Publically available BRGM report - R38894.
Dallinger, R., 1993. Strategies of metal detoxification in terrestrial invertebrates. In R. Dallinger & P. S. Rainbow (eds), Ecotoxicology of Metals in Invertebrates. Lewis Publishers, Boca Raton: 245–289.
Day, K. E. & I. M. Scott, 1990. Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquat. Toxicol. 18: 101–114.
Ellman, G. L., K. D. Courtney, V. Andres & R. M. Featherstone, 1961. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem. Pharmac. 7: 88–95.
Ettajani, H., C. Amiard-Triquet, A. Y. Jeantet & J. C. Amiard, 1996. Fate and effects of soluble or sediment-bound arsenic in oysters (Crassostrea gigas Thun.). Arch. envir. Contam. Toxicol. 31: 38–46.
Fitzpatrick, P. J. & D. Sheehan, 1993. Separation of multiple forms of glutathione S-transferases from the blue mussel, Mytilus edulis. Xenobiotica 23: 851–861.
Galgani, F. & G. Bocquené, 1989. A method for routine determination of organosphosphates and carbamates in sea water. Envir. Technol. Lett. 10: 311–322.
Galzigna, L., G. S. Corsi, B. Saia & A. A. Rizzoli, 1969. Inhibitory effects of triethyl lead on serum cholinesterase in vitro. Clin. Chem. Acta 26: 391–393.
Garcia-Martinez, P., G. W. Winston, C. Metash-Dickey, S. C. M. O'Hara & D. R. Livingstone, 1995. Nitrofurantoinstimulated reactive oxygen species production and genotoxicity in digestive gland microsomes and cytosol of the common mussel (Mytilus edulis L.). Toxicol. Appl. Pharmacol. 131: 332–341.
George, S. G. & J. M. Frazier, 1982. Some aspects of the relationship between tolerance to heavy metal pollution and metabolisms of Cd, Cu and Zn in oysters. Thalassia Jugosl. 18: 203–219.
George, S. G., B. J. S. Pirie, A. R. Cheyne, T. L. Coombs & P. T. Grant, 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.
Habig, W. H., M. J. Pabst & W. B. Jakoby, 1974. The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249: 7130–7139.
Heywood, R., R.W. James, A. E. Street, C. J. Rudd & P. S. I. Barry, 1976. In vitro and in vivo study of the ability of tetraethyl lead to inhibit cholinesterase activity. Toxicol. Lett. 2: 11–16.
Hill, E. F. & W. J. Fleming, 1982. Anticholinesterase poisoning of birds: field monitoring and diagnosis of acute poisoning. Envir. Toxicol. Chem. 1: 27–38.
Hill, I. R., P. Matthiessen & F. Heimbach (eds), 1993. Guidance document on sediment toxicity tests and bioassays for freshwater and marine environments. Proc. SETAC Europe Workshop, Renesse, Netherlands.
His, E., M. N. L. Seaman & R. Beiras, 1997. A simplification of the bivalve embryogenesis and larval development bioassay method for water quality assessment. Wat. Res. 31: 351–355.
Jeantet, A. Y., C. Ballan-Dufrançais & J. L. Martin, 1985. Recherche des mécanismes de détoxication du cadmium par l'huître Crassostrea gigas (Mollusque Bivalve). II. Sites intracellulaires d'accumulation du métal dans les organes absorbants et excréteurs. C. R. Acad. Sci., Paris 301: 177–182.
Jeantet, A. Y., C. Ballan-Dufrançais & A. Anglo, 1997. Atteintes cytologiques chez les bivalves marins. In L. Lagadic, T. Caquet, J. C. Amiard & F. Ramade (eds), Biomarqueurs en Ecotoxicologie - Aspects Fondamentaux. Masson, Paris: 315–354.
Journal Officiel de la République Française, 1995. Arrêté du 25 Juillet 1995 relatif au classement de salubrité et à la surveillance des zones de production et des zones de reparcage des coquillages vivants. Publ. on the 1st of Sept. 1995. République Française, Paris.
Kersten, M. & U. Förstner, 1989. Speciation of trace elements in sediments. In G.E. Batley (ed.), Trace Element Speciation: Analytical Methods and Problems, CRC Press, Inc. Bota Raton, Florida: 245–309.
Klöckner, K., H. Rosental & J. Willführ, 1985. Invertebrate bioassays with North Sea water samples. Structural effects on embryos and larvae of serpulids, oysters and sea urchins. Helgoländer Meeresunters 30: 1–19.
Labrot, F., D. Ribera, M. Saint Denis & J. F. Narbonne, 1996. In vitro and in vivo studies of potential biomarkers of lead and uranium contamination: lipid peroxidation, acetylcholinesterase, catalase and glutathione peroxidase activities in three nonmammalian species. Biomarkers 1: 21–28.
Langston, W. J., 1980. Arsenic in U.K. estuarine sediment and its availability to benthic organisms. J. mar. biol. Ass. U.K. 60: 869–881.
Lebesnerais, C., 1985. Etude expérimentale de la digestion chez l'huître japonaise Crassostrea gigas (Thunberg). Thèse de doctorat, Université de Caen, Fr.
Letellier, M., H. Budzinski, P. Garrigues & S. Wise, 1996/1997. Focused microwave assisted extraction of polycyclic aromatic hydrocarbons in open cell from reference materials (sediment, soil, air particulates). Spectroscopy: An International Journal 13: 71–80.
Lowry, O. H., N. J. Rosenbrough, A. I. Farr & R. J. Randall, 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193: 265–275.
Morel, F. M. M. & J. G. Hering, 1993. Principles and applications of aquatic chemistry. John Wiley and Sons. Inc.
Narbonne, J. F., 1991. Mécanismes de biotransformation des polluants organiques chez les animaux marins. Océanis 17: 449–458.
Narbonne, J. F. & P. D. Hansen, 1996. Recent studies on biomarkers on coastal areas: assessment of ecosystem health - ecotoxicological studies. Proceedings of international conference on animal physiology, Münster/Westphalia, May 31-June 2, 1996.
Olson, D. & G. M. Christensen, 1980. Effects of water pollutants and other chemicals on fish acetylcholinesterase (in vitro). Envir. Res. 21: 327–335.
Pellerin-Massicotte, J., 1997. Influence of elevated temperature and air-exposure on MDA levels and catalase activities in digestive glands of the blue mussel (Mytilus edulis L.). J. Rech. Océanogr. 22: 91–98.
Pellerin-Massicotte, J., 1994. Oxidative processes as indicators of chemical stress in marine bivalves. J. aquat. Ecos. Health 3: 101–111.
Pirie, B. J. S., S. G. George, D. G. Lytton & J. D. Thomson, 1984. Metal-containing blood cells of oysters: ultrastructure, histochemistry and X-ray microanalysis. J. mar. biol. Ass. U.K. 64: 115–123.
R.N.O., 1995. Surveillance du milieu marin. Ministère de l'Environnement, 32 pp.
Rainbow P. S., 1993. The significance of trace metal concentrations in marine Invertebrates. In R. Dallinger & P. S. Rainbow (eds), Ecotoxicology of Metals in Invertebrates. Lewis Publishers, Boca Raton: 3–23.
Regoli, F. & G. Principato, 1995. Glutathione, glutathionedependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical markers. Aquat. Toxicol. 31: 143–164.
Ringwood, A. H. & M. Brouwer, 1995. Patterns of metallothionein expression in oyster embryos. Mar. Envir. Res. 39: 101–105.
Salomons, W. & U. Forstner, 1980. Trace metals analysis on polluted sediments. Envir. Techn. Lett. 1: 506–517.
Shannon, R. D. & J. R. White, 1991. The selectivity of a sequential extraction procedure for the determination of iron oxyhydroxides and iron sulfides in lake sediments. Biogeochem. 14: 193–208.
Schmidt, G. H. & N. M. M. Ibrahim, 1994. Heavy metal content (Hg2+, Pb2+) in various body parts: its impact on cholinesterase activity and binding glycoproteins in the grasshopper Aiolopus thalassinus adults. Ecotox. envir. Saf. 29: 148–164.
Sokal, R. R. & F. J. Rohlf, 1981. Biometry. Freeman, New York.
Suszkiw, J., G. Toth, M. Murawsky & G. P. Cooper, 1984. Effects of Pb2+ and Cd2+ on acetylcholine release and Ca2+ movements in synaptosomes and subcellular fractions from rat brain and Torpedo Electric Organ. Brain Res. 323: 31–46.
Tessier, A., P. G. C. Campbell & M. Bisson, 1979. Sequential extraction procedure for the speciation of particulate trace metals. Anal. Chem. 51: 844–851.
Tessier, A., P. G. C. Campbell, J. C. Auclair & M. Bisson, 1984. Relationships between the partitioning of trace metals in sediments and their accumulation in the tissues of the freshwater mollusc Elliptio complanata in a mining area. Can. J. Fish. aquat. Sci. 41: 1463–1472.
Thompson, J. A. J. & R. P. Cosson, 1984. An improved electrochemical method for the quantification of metallothioneins in marine organisms. Mar. Envir. Res. 11: 137–152.
Thompson, J. D., B. J. S. Pirie & S. G. George, 1985. Cellular metal distribution in the Pacific Oyster, Crassostrea gigas (Thun.) determined by quantitative X-ray microprobe analysis. J. exp. mar. Biol. Ecol. 85: 37–45.
Viarengo, A., L. Canesi, M. Pertica & D. R. Livingstone, 1991. Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comp. Biochem. Physiol. 100C: 187–190.
Viarengo, A., L. Canesi, M. Pertica, G. Poli, M. N. Moore & M. Orunesu, 1990. Heavy metal effects on lipids peroxidation in the tissues of Mytilus galloprovincialis Lam. Comp. Biochem. Physiol. 97C: 37–42.
Rights and permissions
About this article
Cite this article
Amiard-Triquet, C., Altmann, S., Amiard, J.C. et al. Fate and effects of micropollutants in the Gironde estuary, France: a multidisciplinary approach. Hydrobiologia 373, 259–279 (1998). https://doi.org/10.1023/A:1017055118218
Issue Date:
DOI: https://doi.org/10.1023/A:1017055118218