Comparative study of the accumulation and detoxification of Cu (essential metal) and Hg (nonessential metal) in the digestive gland and gills of mussels Mytilus galloprovincialis, using analytical and histochemical techniques

Chemosphere

Volumn 83, Issue 8, 2011, Pages 1155-1165

  Raftopoulou, E K ^a   Dimitriadis, V K ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

Author keywords

Accumulation; Copper; Detoxification; Mercury; Mytilus galloprovincialis

Indexed keywords

COPPER; DETOXIFICATION; HEAVY METALS; HISTOLOGY; MERCURY (METAL); MIXTURES; MOLLUSCS; SILVER DEPOSITS; SPECTROPHOTOMETRY; TISSUE;

ACCUMULATION; ANTAGONISTIC EFFECTS; ATOMIC ABSORPTION SPECTROPHOTOMETRY; COMPARATIVE STUDIES; DIGESTIVE GLANDS; ESSENTIAL METALS; LABORATORY CONDITIONS; MYTILUS GALLOPROVINCIALIS;

DIGESTIVE SYSTEM;

COPPER; MERCURY;

ATOMIC ABSORPTION SPECTROSCOPY; BIOACCUMULATION; BIVALVE; COMPARATIVE STUDY; COPPER; DETOXIFICATION; HISTOLOGY; MERCURY (ELEMENT); POLLUTION EXPOSURE; TOXICITY;

ANIMAL TISSUE; ARTICLE; ATOMIC ABSORPTION SPECTROMETRY; AUTOMETALLOGRAPHY; COMPARATIVE STUDY; COPPER METABOLISM; DETOXIFICATION; EXOCRINE GLAND; GILL; HISTOCHEMISTRY; LYSOSOME; MERCURIALISM; MYTILUS GALLOPROVINCIALIS; NONHUMAN;

ANIMALIA; MYTILUS GALLOPROVINCIALIS;

EID: 79955004716     PISSN: 00456535     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chemosphere.2011.01.003     Document Type: Article

References (76)

1. Amiard J.C., Amiard-Triquet C., Berthert B., Metayer C. Comparative study of the patterns of bioaccumulation of essential (Cu, Zn) and nonessential (Cd, Pb) trace metals in various estuarine and coastal organisms. J. Exp. Mar. Biol. Ecol. 1987, 106:73-89.
2. Amiard J.C., Amiard-Triquet C., Barka S., Pellerin J., Rainbow P.S. Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 2006, 76(2):160-202.
3. Anandraj A., Marshall D.J., Gregory M.A., McClurg T.P. Metal accumulation, filtration and O2 uptake rates in the mussel Perna perna (Mollusca: Bivalvia) exposed to Hg+, Cu2+, and Zn2+. Comp. Biochem. Physiol. C. Toxicol. Pharmacol. 2002, 132(3):355-363.
4. Balogh V.K., Salanki J. Biological monitoring of heavy metal pollution in the region of lake Balaton (Hungary). Acta Biol. Hung. 1987, 38(1):13-30.
5. Barnes H., Stanbury F.A. The toxic action of copper and mercury salts both separately and when mixed on the herpacticoid copepod Nitocra spinipes (Boeck). J. Exp. Biol. 1948, 25:270-275.
6. Bayne B.L., Brown D.A., Harrison F.L., Yevich P.D. Mussel health. The International Mussel Watch 1980, 163-235. National Academy of Sciences, Washington, DC. E.D. Goldberg (Ed.).
7. Boisson F., Hartl M.G.J., Fowler S.W., Amiard-Triquet C. Influence of chronic exposure to silver and mercury in the field on the bioaccumulation potential of the bivalve Macoma balthica. Mar. Environ. Res. 1998, 45:325-340.
8. Burlando B., Viarengo A., Pertica M., Mancinelli G., Marchi B., Orunesu M. Effects of Hg 2+ on Ca2+ dynamics in the scallop sarcoplasmic reticulum (Pecten jacobaeus): protective role of glutathione. Comp. Biochem. Physiol. 1997, 116C:77-83.
9. Calow P. Heavy metals. Handbook of Ecotoxicology 1994, vol. 2. Oxford Blackwell Scientific Publications, London, pp. 79-97.
10. Chatziargyriou V., Dailianis S. The role of selenium-dependent glutathione peroxidase (Se-GPx) against oxidative and genotoxic effects of mercury in haemocytes of mussel Mytilus galloprovincialis (Lmk.). Toxicol. In Vitro 2010, 24:1363-1372.
11. Chavez-Crooker P., Garrido N., Pozo P., Ahearn G.A. Copper transport by lobster (Homarus americanus) hepatopancreatic lysosomes. Comp. Biochem. Physiol. 2003, 135C:107-118.
12. Clark, R.B., 1996. Metals. Marine Pollution. Oxford University Press, Oxford, New York, pp. 64-82 (Chapter 5).
13. Cossa, D., Laurier, F.J.G., Ficht, A., 2002. Mercury contamination in the Seine estuary, France: an overview. In: Cai, Y., Braids, O.C. (Eds.), Biochemistry of Environmentally Important Elements. American Chemical Society, Washington, DC, pp. 298-320 (Chapter 20).
14. Da Ros L., Nasci C., Marigómez I., Soto M. Biomarkers and trace metals in the digestive gland of indigenous and transplanted mussels, Mytilus galloprovincialis in Venice lagoon, Italy. Mar. Environ. Res. 2000, 50:417-423.
15. Da Ros L., Meneghetti F., Nasci C. Field application of lysosomal destabilisation indices in the mussel Mytilus galloprovincialis: biomonitoring and transplantation in the Lagoon of Venice (North-East Italy). Mar. Environ. Res. 2002, 54:817-822.
16. Danscher G. Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electron microscopy. Histochemistry 1981, 71:1-16.
17. Danscher G. Autometallography. A new technique for light and electron microscopic visualization of metals in biological tissue (gold, silver, metal sulfides and metal selenides). Histochemistry 1984, 81:331-335.
18. Danscher G., Montagnese C. Autometallographic localization of synaptic vesicular zinc and lysosomal gold, silver and mercury. J. Histotechnol. 1994, 17:15-22.
19. Depledge M.H., Rainbow P.S. Models of regulation and accumulation of trace metals in marine invertebrates (mini review). Comp. Biochem. Physiol. C 1990, 97:1-7.
20. Dimitriadis V.K., Domouhtsidou G.P., Raftopoulou E. Localization of Hg and Pb in the palps, the digestive gland and the gills in Mytilus galloprovincialis (L.) using autometallography and X-ray microanalysis. Environ. Pollut. 2003, 125:345-353.
21. Domouhtsidou G.P., Dimitriadis V.K. Ultrastructural localization of heavy metals (Hg, Ag, Pb and Cu) in gills and digestive gland of mussels Mytilus galloprovincialis (L.). Arch. Environ. Contam. Toxicol. 2000, 38:472-478.
22. Engel D.W., Sunda W.G. Toxicity of cupric ion to eggs of the spot Leiostomus xanthurus and the Atlantic silverside Menidia menidia. Mar. Biol. 1979, 50:121-126.
23. Etxeberria M., Sastre I., Cajaraville M.P., Marigómez I. Digestive lysosome enlargement induced by experimental exposure to metals (Cu, Cd and Zn) in mussels collected from a zinc-polluted site. Arch. Environ. Contam. Toxicol. 1994, 27:338-345.
24. Faria M., Carrasco L., Diez S., Riva M.C., Bayona J.M., Barata C. Multi-biomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals. Comp. Biochem. Physiol. Part C 2009, 149(3):281-288.
25. Fernandez N., Beiras R. Combined toxicity of dissolved mercury with copper, lead and cadmium on embryogenesis and early larval growth of the Paracentrotus lividus sea-urchin. Ecotoxicology 2001, 10:263-271.
26. Fischer H. Shell weight as an independent variable in relation to cadmium balance content of mollusks. Mar. Ecol. Prog. Ser. 1983, 12:59-75.
27. Fischer H. Influence of temperature, salinity and oxygen on the cadmium balance of mussels Mytilus edulis. Mar. Ecol. Prog. Ser. 1986, 32:265-278.
28. George S.G., Coombs T.L. The effects of chelatin agents on the uptake and accumulation of cadmium by Mytilus edulis. Mar. Biol. 1977, 39:261-278.
29. George S.G., Pirie B.J.S., Cheyne A.R., Coombs T.L., Grant P.T. Detoxification of metals by marine bivalves: an ultrastructural study of the compartmentation of copper and zinc in the oyster Ostrea edulis. Mar. Biol. 1978, 45:147-156.
30. Giamberini L., Auffret M., Pihan J.C. Hemocytes of the freshwater mussel, Dreissena polymorpha Pallas: cytology, cytochemistry and X-ray microanalysis. J. Moll. Stud. 1996, 62:367-379.
31. Herwig H.J., Brands F., Kruitwagen E., Zandee D.I. Bioaccumulation and histochemical localization of cadmium in Dreissena polymorpha exposed to cadmium chloride. Aquat. Toxicol. 1989, 15:269-286.
32. Jing G., Li Y., Xie L., Zhang R. Metal accumulation and activities in gills and digestive gland of pearl oyster (Pinctata fucata) exposed to copper. Comp. Biochem. Physiol. C 2006, 144:184-190.
33. Kagi J.H.R., Hapke H.J. Biochemical interactions of mercury, cadmium and lead. Changing Metal Cycles and Human Health 1984, 237-250. Springer-Verlag, Berlin. J.O. Nriagu (Ed.).
34. Landrum P.F., Harkey G.A., Kukkonen J. Evaluation of organic contaminant exposure in aquatic organisms: the significance of bioconcentration and bioaccumulation. Ecotoxicology: A Hierarchical Treatment 1996, 85-131. Lewis Publishers, Tokyo. M.C. Newman, C.H. Jagoe (Eds.).
35. Langston W.J., Spence S.K. Biological factors involved in metal concentrations observed in aquatic organisms. Metal Speciation and Bioavailability in Aquatic Systems 1995, 407-478. John Wiley, Chichester, UK. A. Tessier, D.R. Turner (Eds.).
36. Lorenzo J.I., Beiras R., Mubiana V.K., Blust R. Copper uptake by Mytilus edulis in the presence of humic acids. Environ. Toxicol. Chem. 2005, 24(4):973-980.
37. MacInnes, J.R., Calabrese, J., 1978. Response of embryos of the American Oyster, Crassostrea virginica, to heavy metals at different temperatures. In: McLusky, D.S., Berry, A.J., (Eds.), Physiology and Behavior of Marine Organisms. Pergamon Press, New York, NY, pp. 195-202.
38. Marigomez I., Baybay-Villacorta L. Pollutant-specific and general lysosomal responses in digestive cells of mussels exposed to model organic chemicals. Aquat. Toxicol. 2003, 64(3):235-257.
39. Marigomez J.A., Cajaraville M.P., Angulo E. Cellular distribution of cadmium in the common winkle Littorina littorea (L.) determined by X-ray microprobe analysis and histochemistry. Histochemistry 1990, 94:191-199.
40. Marigómez I., Cajaraville M.P., Soto M., Lekube X. Cell-type replacement, a successful strategy of molluscs to adapt to chronic exposure to pollutants. Cuad. Invest. Biol. 1998, 20:411-414.
41. Marigómez I., Soto M., Cajaraville M.P., Angulo E., Giamberini L. Cellular and subcellular distribution of metals in molluscs. Microsc. Res. Tech. 2002, 56:358-392.
42. Marigómez I., Izagirre U., Lekube X. Lysosomal enlargement in digestive cells of mussels exposed to cadmium, benzo[a]pyrene and their combination. Comp. Biochem. Physiol. C 2005, 141:188-193.
43. Marin M.G., Boscolo R., Cella A., Degetto S., Da Ros L. Field validation of autometallographical black silver deposit (BSD) extent in three bivalve species from the Lagoon of Venice, Italy (Mytilus galloprovincialis, Tapes philippinarum, Scapharca inaequivalvis) for metal bioavailability assessment. Sci. Total. Environ. 2006, 371(1-3):156-167.
44. Mason A.Z., Simkiss K. Interactions between metals and their distribution in tissues of Littorina littorea (L.) collected from clean and polluted sites. J. Mar. Biol. Assoc. U. K. 1983, 63:661-672.
45. Metian M., Warnau M., Cosson R.P., Oberhansli F., Bustamante P. Bioaccumulation and detoxification processes of Hg in the king scallop Pecten maximus: field and laboratory investigations. Aquat. Toxicol. 2008, 90:204-213.
46. Moore M.N. Cytochemical demonstration of latency of lysosomal hydrolases in digestive cells of the common mussel Mytilus edulis and changes induced by thermal stress. Cell. Tissue Res. 1976, 175(3):279-287.
47. Moore M.N. Cellular responses to pollutants. Mar. Pollut. Bull. 1985, 16:134-139.
48. Moore M.N. Cytochemical responses of the lysosomal system and NADPH-ferrihemoprotein reductase in molluscan digestive cells to environmental and experimental exposure to xenobiotics. Mar. Ecol. Prog. Ser. 1988, 46:81-89.
49. Moulder S.M. Combined effect of the chlorides of mercury and copper in sea water on the euryhaline amphipod Gammarus duebeni. Mar. Biol. 1980, 59(4):193-200.
50. Murakkami T.H., Fujii T., Hara T., Fishida A. The effects of heavy metals on developing sea urchin eggs. J. Okayama Med. Soc. 1976, 88:39-50.
51. Nicholson S. Lysosomal membrane stability, phagocytosis and tolerance to emersion in the mussel Perna viridis (Bivalvia: Mytilidae) following exposure to acute, sublethal, copper. Chemosphere 2003, 52:1147-1151.
52. Nolan C., Duke E., Lorenzon G., Sabbioni E., Marafante E. Heavy metal uptake and intracellular binding in isolated gill preparations of Mytilus galloprovincialis L. Sci. Total Environ. 1984, 40:83-92.
53. Pereira S.A., Nascimento A., Smith H., Leite N.L., de Araujo M.S., Silva A. The combined effects of temperature and metals copper, zinc and mercury on the embryological development of the mangrove oyster Crassostrea rhizophorae. Ecotoxicol. Environ. Restorat. 1998, 1(1):21-32.
54. Phillips D.G.H. Quantitative Aquatic Biological Indicators: Their use to Monitor Trace Metal and Organochlorine Pollution 1980, Applied Science Publishers, Ltd, London.
55. Porte C., Biosca X., Sole M., Albaiges J. The integrated use of chemical analysis, cytochrome P450 and stress proteins in mussels to assess pollution along the Galician coast (NW Spain). Environ. Pollut. 2001, 112:261-268.
56. Prato E., Biandolino F. Combined toxicity of mercury, copper and cadmium on embryogenesis and early larval stages of the Mytilus galloprovincialis. Environ. Technol. 2007, 28:915-920.
57. Raftopoulou E.K., Domouhtsidou G.P., Dimitriadis V.K. Autometallographic localization of heavy metals in resin sections cryosections and isolated cells of the mussel Mytilus galloprovincialis (L.). Histochem. J. 2002, 34:583-588.
58. Rajalaksmi S., Mohandas A. Copper-induced changes in tissue enzyme activity in a freshwater mussel. Ecotoxicol. Environ. Saf. 2005, 62:140-143.
59. Regoli F. Lysosomal responses as sensitive stress index in biomonitoring heavy metal pollution. Mar. Ecol. Prog. Ser. 1992, 84:63-69.
60. Regoli F. Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean mussel Mytilus galloprovincialis. Arch. Environ. Contam. Toxicol. 1998, 34:48-63.
61. Regoli F., Orlando E., Mauri M., Nigro M., Cognetti G.A. Heavy metal accumulation and calcium content in the bivalve Donacilla cornea. Mar. Ecol. Prog. Ser. 1991, 74:219-224.
62. Rivaro P., Ianni C., Abelmoschi M.L., Soggia F., Frache R. Laboratory studies on the accumulation of inorganic mercury and methylmercury by the mussel (Mytilus galloprovincialis, Lam) in relation to the presence of sediment. Toxicol. Environ. Chem. 2009, 91(6):1159-1173.
63. Roesijadi G., Fellingham G.W. Influence of Cu, Cd and Zn pre-exposure on Hg toxicity in the mussel Mytilus edulis. Can J. Fish Aquat. Sci. 1987, 44:680-684.
64. Roesijadi G., Drum A.S., Thomas J.T., Fellingham G.W. Enhanced mercury tolerance in marine mussels and relationship to low molecular weight, mercury-binding proteins. Mar. Pollut. Bull. 1982, 13:250-253.
65. Serafim A., Bebianno M.J. Effect of a polymetallic mixture on metal accumulation and metallothionein response in the clam Ruditapes decussatus. Aquat. Toxicol. 2010, 99:370-378.
66. Shi D., Wang W.X. Modification of trace metal accumulation in the green mussel Perna viridis by exposure to Ag, Cu and Zn. Environ. Pollut. 2004, 132:265-277.
67. Soto M., Marigomez I. BSD extent, an index for metal pollution screening based on the metal content within digestive cell lysosomes of mussels as determined by autometallography. Ecotoxicol. Environ. Saf. 1997, 37:141-151.
68. Soto M., Cajaraville M.P., Angulo E., Marigomez I. Autometallographic localization of protein-bound cooper and zinc in the common winkle, Littorina littorea: a light microscopical study. Histochem. J. 1996, 28:689-701.
69. Soto M., Cajaraville M.P., Angulo E., Marigomez I. Tissue and cell distribution of copper, zinc and cadmium in the mussel Mytilus galloprovincialis, determined by autometallography. Tissue Cell. 1996, 28(5):557-568.
70. Soto M., Zaldibar B., Cancio I., Taylor M.G., Turner M., Morgan A.J., Marigómez I. Subcellular distribution of cadmium and its cellular ligands in mussel digestive gland cells as revealed by combined autometallography and X-ray microprobe analysis. Histochem. J. 2002, 34:273-280.
71. Sunda W.G., Guillard R.R. The relationship between cupric ion activity and the toxicity of copper to phytoplankton. J. Mar. Res. 1976, 34:511-529.
72. UNEP/RAMOGE, 1999. Manual on the Biomarkers Recommended for the MED POL Biomonitoring Programme, UNEP, Athens.
73. Verlecar X.N., Jena K.B., Chainy G.B.N. Modulation of antioxidant defences in digestive gland of Perna viridis (L.), on mercury exposures. Chemosphere 2008, 71(10):1977-1985.
74. Viarengo A., Zanicchi G., Moore M.N., Orunesu M. Accumulation and detoxification of copper by the mussel Mytilus galloprovincialis Lam: a study of subcellular distribution in the digestive gland cells. Aquat. Toxicol. 1981, 1:147-157.
75. Ward R.E. Metal concentrations and digestive gland lysosomal stability in mussels from Halifax Inlet, Canada. Mar. Pollut. Bull. 1990, 21:237-240.
76. Widdows J., Bayne B.L., Donkin P., Livingstone D.R., Lowe D.M., Moore M.N., Salkeld P.N. Measurement of the responses of mussels to environmental stress and pollution at Sullon Voe: a based-line study. Proc. R. Soc. Edinburgh 1981, 80:323-383.