Heavy metal contamination and hepatic toxicological responses in brown trout (Salmo trutta) from the Kerguelen Islands

References

• Abollino O., Aceto M., Buoso S., Gasparon M., Green W.J., Malandrino M., Mentasti E. Distribution of major, minor and trace elements in lake environments of Antarctica. Antarctic Science. 2004; 16: 277–291.
   Web of Science ®Google Scholar
• Adams S.M., Ham K.D., Greeley M.S., LeHew R.F., Hinton D.E., Saylor C.F. Downstream gradients in bioindicator responses: point source contaminant effects on fish health. Canadian Journal of Fisheries and Aquatic Sciences. 1996; 53: 2177–2187.
   Web of Science ®Google Scholar
• Agius C. Preliminary studies on the ontogeny of the melano-macrophages of teleost haemopoietic tissues and age-related changes. Developmental and Comparative Immunology. 1981; 5: 597–606.
   PubMed Web of Science ®Google Scholar
• Ait-Aissa S., Ausseil O., Palluel O., Vindimian E., Garnier-Laplace J., Porcher J.M. Biomarker responses in juvenile rainbow trout (Oncorhynchus mykiss) after single and combined exposure to low doses of cadmium, zinc, PCB77 and 17ß-oestradiol. Biomarkers. 2003; 8: 491–508.
   PubMed Web of Science ®Google Scholar
• Amundsen P.-A., Staldvik F.J., Lukin A.A., Kashulin N.A., Popova O.A., Reshetnikov Y.S. Heavy metal contamination in freshwater fish from the border region between Norway and Russia. Science of the Total Environment. 1997; 201: 211–224.
   PubMed Web of Science ®Google Scholar
• Babo S., Vasseur P. In vitro effects of Thiram on liver antioxidant enzyme activities of rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology. 1992; 22: 61–68.
   Web of Science ®Google Scholar
• Bargagli R. Environmental contamination in Antarctic ecosystems. Science of the Total Environment. 2008; 400: 212–226.
   PubMed Web of Science ®Google Scholar
• Baysoy E., Atli G., Gürler C., Dogan Z., Eroglu A., Kocalar K., Canli M. The effects of increased freshwater salinity in the biodisponibility of metals (Cr, Pb) and effects on antioxidant systems of Oreochromis niloticus. Ecotoxicology and Environmental Safety. 2012; 84: 249–253.
   PubMed Web of Science ®Google Scholar
• Bernet D., Schmidt-Posthaus H., Wahli T., Burkhardt-Holm P. Evaluation of two monitoring approaches to assess effects of waste water disposal on histological alterations in fish. Hydrobiologia. 2004; 524: 53–66.
   Web of Science ®Google Scholar
• Betoulle S., Duchiron C., Deschaux P. Lindane increases in vitro respiratory burst activity and intracellular calcium levels in rainbow trout (Oncorhynchus mykiss) head kidney phagocytes. Aquatic Toxicology. 2000; 48: 211–221.
   PubMed Web of Science ®Google Scholar
• Biagianti-Risbourg S. Contribution à l’étude du foie de juvéniles de muges (Téléostéens, Mugilides), contaminés expérimentalement par l'atrazine (s-triazine herbicide): approche ultrastructurale et métabolique: intérêt en écotoxicologie. (Study of juveniles mullet [Teleostei, Mugilidae] liver contaminated by atrazine [s-triazine herbicide]: ultrastructural and metabolic approach: ecotoxicological interest.). 1990; University of Perpignan. PhD thesis.
   Google Scholar
• Borucinska J.D., Kotran K., Shackett M., Barker T. Melanomacrophages in three species of free-ranging sharks from the northwestern Atlantic, the blue shark Prionacae glauca (L.), the shortfin mako, Isurus oxyrhinchus Rafinesque, and the thresher, Alopias vulpinus (Bonnaterre). Journal of Fish Diseases. 2009; 32: 883–891.
   Web of Science ®Google Scholar
• Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry. 1976; 72: 248–254.
   PubMed Web of Science ®Google Scholar
• Braunbeck T. Braunbeck D.E. Cytological alterations in fish hepatocytes following in vivo sublethal exposure to xenobiotics—structural biomarkers of environmental contamination. Fish ecotoxicology. 1998; Berlin: Springer. 61–140.
   Google Scholar
• Broeg K. The activity of macrophage aggregates in the liver of flounder (Platichthys flesus) and wrasse (Symphodus melops) is associated with tissue damage. Marine Environmental Research. 2010; 69: S14–S16.
   Web of Science ®Google Scholar
• Bruslé J., Anadon G.G. Datta-Munshi J.S., Dutta H.M. The structure and function of fish liver. Fish morphology. 1996; Boca Raton, FL: CRC Press. 77–93.
   Google Scholar
• Bruslé J., Quignard J.P. Biologie des poissons d'eau douce européens. (Biology of European freshwater fish.). 2001; Paris: Lavoisier.
   Google Scholar
• Bryère P., Charrier M. Variations du régime alimentaire en fonction de l'habitat de la truite commune (Salmo trutta L.) introduite dans l'Archipel de Kerguelen. (Diet variations depending on the habitat of brown trout [Salmo trutta L.] introduced into the Kerguelen archipelago.). 2009. Master's thesis, Rennes 1 University, Rennes, France.
   Google Scholar
• Bustamante P., Bocher P., Chérel Y., Miramand P., Caurant F. Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands. The Science of the Total Environment. 2003; 313: 25–39.
   PubMed Web of Science ®Google Scholar
• Bustamante P., Cherel Y., Caurant F., Miramand P. Cadmium, copper and zinc in octopuses from Kerguelen Islands, southern Indian Ocean. Polar Biology. 1998; 19: 264–271.
   Web of Science ®Google Scholar
• Carrola J., Fontainhas-Fernandes A., Matos P., Rocha E. Liver histopathology in brown trout (Salmo trutta f. fario) from the Tinhela River, subjected to mine drainage from the abandoned Jales Mine (Portugal). Bulletin of Environmental Contamination and Toxicology. 2009; 83: 35–41.
   Web of Science ®Google Scholar
• Cazenave J., Bacchetta C., Rossi A., Ale A., Campana M., Parma M.J. Deleterious effects of wastewater on the health status of fish: a field caging study. Ecological Indicators. 2014; 38: 104–112.
   Web of Science ®Google Scholar
• Davaine P., Beall E., Guerri O., Caraguel J.M. Salmonid introductions into virgin ecosystems (Kerguelen islands, Subantarctic): stakes, results, prospects. Bulletin Français de la Pêche et de la Pisciculture. 1997; 344/345: 93–110.
   Google Scholar
• EU. Directive 2006/44/EC of the European Parliament and of the Council of 6 September 2006 on the quality of fresh waters needing protection or improvement in order to support fish life. 2006. Accessed on the internet at http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:32006L0044 on 1 July 2013..
   Google Scholar
• Evans M.S., Muir D., Lockhart W.L., Stern G., Ryan M., Roach P. Persistent organic pollutants and metals in the freshwater biota of the Canadian Subarctic and Arctic: an overview. Science of the Total Environment. 2005; 351/352: 94–147.
   Web of Science ®Google Scholar
• Farkas A., Salánki J., Specziár A. Age- and size-specific patterns of heavy metals in the organs of freshwater fish Abramis brama L. populating a low-contaminated site. Water Research. 2003; 37: 959–964.
   PubMed Web of Science ®Google Scholar
• Fernández J.A., Vázquez M.D., López J., Carballeira A. Modelling the extra and intracellular uptake and discharge of heavy metals in Fontinalis antipyretica transplanted along a heavy metal and pH contamination gradient. Environmental Pollution. 2006; 139: 21–31.
   PubMed Web of Science ®Google Scholar
• Gay C. Ecologie du zooplancton d'eau douce des Iles Kerguelen. Caractéristiques du milieu et inventaire des entomostracés. (Ecology of freshwater zooplankton of the Kerguelen Islands. Environmental characteristics and entomostraca inventory.). CNFRA. 1981; 47: 43–57.
   Google Scholar
• Greenfield B.K., Teh S.J., Ross J.R.M., Hunt J., Zhang G., Davis J.A., Ichikawa G., Crane D., Hung S.S.O., Deng D., Teh F.C., Green P.G. Contaminant concentrations and histopathological effects in Sacramento splittail (Pogonichthys macrolepidotus). Archives of Environmental Contamination and Toxicology. 2008; 55: 270–281.
   PubMed Web of Science ®Google Scholar
• Gül Ş., Belge-Kurutaş E., Yıldız E., Şahan A., Doran F. Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environment International. 2004; 30: 605–609.
   PubMed Web of Science ®Google Scholar
• Hinton D.E., Laurén D.J. McCarty J.F., Shugart L.R. Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. Biomarkers of environmental contamination. 1990; Boca Raton, FL: Lewis Publishers. 15–57.
   Google Scholar
• Jaffal A., Givaudan N., Betoulle S., Terreau A., Paris-Palacios S., Biagianti-Risbourg S., Beall E., Roche H. Polychlorinated biphenyls in freshwater salmonids from the Kerguelen Islands in the Southern Ocean. Environmental Pollution. 2011; 159: 1381–1389.
   PubMed Web of Science ®Google Scholar
• Jaffal A., Paris-Palacios S., Jolly S., Thailly A., Delahaut L., Beall E., Roche H., Biagianti-Risbourg S., Betoulle S. Cadmium and copper contents in a freshwater fish species (brook trout, Salvelinus fontinalis) from the Subantarctic Kerguelen Islands. Polar Biology. 2011; 34: 397–409.
   Web of Science ®Google Scholar
• Johnson J.C., Nettikadan S.R., Vengasandra S.G., Lovan S., Muys J., Henderson E., Christiansen J. Characterization of testudine melanomacrophage linear, membrane extension processes—cablepodia—by phase and atomic force microscopy. In Vitro Cellular and Developmental Biology—Animal. 2005; 41: 225–231.
   Web of Science ®Google Scholar
• Kojadinovic J., Potier M., Le Corre M., Cosson R.P., Bustamante P. Bioaccumulation of trace elements in pelagic fish from the Western Indian Ocean. Environmental Pollution. 2007; 146: 548–566.
   PubMed Web of Science ®Google Scholar
• Kolayli S., Keha E. A comparative study of antioxidant enzyme activities in freshwater and seawater-adapted rainbow trout. Journal of Biochemical and Molecular Toxicology. 1999; 13: 334–37.
   PubMed Web of Science ®Google Scholar
• Lagadic L., Caquet T., Amiard J.C. Lagadic L. Biomarqueurs en écotoxicologie: principes et définitions. (Biomarkers in ecotoxicology: principles and definitions.). Biomarqueurs en écotoxicologie. Aspects fondamentaux. (Biomarkers in ecotoxicology. Fundamental aspects.). 1997; Paris: Masson. 1–9.
   Google Scholar
• Lamas S., Fernández J.A., Aboal J.R., Carballeira A. Testing the use of juvenile Salmo trutta L. as biomonitors of heavy metal pollution in freshwater. Chemosphere. 2007; 67: 221–228.
   Web of Science ®Google Scholar
• Loizeau V., Abarnou A. Distribution of polychlorobiphenyls in dab (Limanda limanda) from the Baie de Sein (Eastern Channel). Marine Environmental Research. 1994; 38: 77–91.
   Web of Science ®Google Scholar
• Manera M., Serra R., Isani G., Carpené E. Macrophage aggregates in gilthead sea bream fed copper, iron and zinc enriched diets. Journal of Fish Biology. 2000; 57: 457–465.
   Web of Science ®Google Scholar
• Marchand M.J., Van Dyk J.C., Pieterse G.M., Barnhoorn I.E.J., Bornman M.S. Histopathological alterations in the liver of the sharptooth catfish Clarias gariepinus from polluted aquatic systems in South Africa. Environmental Toxicology. 2009; 24: 133–147.
   PubMed Web of Science ®Google Scholar
• Mayon N., Bertand A., Leroy D., Malbrouck C., Mandiki S.N.M., Silvestre F., Goffard A., Thome J.P., Kestemont P. Multiscale approach of fish responses to different types of environmental contaminations: a case study. Science of the Total Environment. 2006; 367: 715–731.
   Web of Science ®Google Scholar
• Moore J.N., Luoma S.N., Peters D. Downstream effects of mine effluent on an intermontane riparian system. Canadian Journal of Fisheries and Aquatic Sciences. 1991; 48: 222–232.
   Web of Science ®Google Scholar
• Morat F., Betoulle S., Robert M., Thailly A.F., Biagianti-Risbourg S., Lecomte-Finiger R. What can otolith examination tell us about the level of perturbations of salmonid fish from the Kerguelen Islands?. Ecology of Freshwater Fish. 2008; 17: 617–627.
   Web of Science ®Google Scholar
• Paoletti F., Aldinucci D., Mocali A., Caparrini A. A sensitive spectrophotometric method for the determination of superoxide dismutase activity in tissue extracts. Analytical Biochemistry. 1986; 154: 536–541.
   PubMed Web of Science ®Google Scholar
• Paris-Palacios S., Biagianti-Risbourg S. Hepatocyte nuclear structure and subcellular distribution of copper in zebrafish Brachydanio rerio and roach Rutilus rutilus (Teleostei, Cyprinidae) exposed to copper sulphate. Aquatic Toxicology. 2006; 77: 306–313.
   Web of Science ®Google Scholar
• Paris-Palacios S., Biagianti-Risbourg S., Vernet G. Hepatic disorders induced by a sublethal concentration of procymidone (fongicide dicarboximide) in Brachydanio rerio (teleostei, cyprinidae): histo-cytological approach. Bulletin Français de la Pêche et de la Protection des Milieux Aquatiques. 1998; 71: 547–562.
   Google Scholar
• Paris-Palacios S., Biagianti-Risbourg S., Vernet G. Biochemical and (ultra)structural hepatic perturbations of Brachydanio rerio (Teleostei, Cyprinidae) exposed to two sublethal concentrations of copper sulfate. Aquatic Toxicology. 2000; 50: 109–124.
   PubMed Web of Science ®Google Scholar
• Peute J., Huiskamp R., Van Oordt P. Quantitative analysis of estradiol-17β-induced changes in the ultrastructure of the liver of the male zebrafish, Brachydanio rerio. Cell and Tissue Research. 1985; 242: 377–382.
   Web of Science ®Google Scholar
• Sanchez W., Ait-Aissa S., Palluel O., Ditche J.M., Porcher J.M. Preliminary investigation of multi-biomarker responses in three-spined stickleback (Gasterosteus aculeatus L.) sampled in contaminated streams. Ecotoxicology. 2007; 16: 279–287.
   PubMed Web of Science ®Google Scholar
• Sanchez W., Palluel O., Lagadic L., Ait-Aissa S., Porcher J.M. Biochemical effects of nonylphenol polyethoxylate adjuvant, Diquat herbicide and their mixture on the three-spined stickleback (Gasterosteus aculeatus L.). Marine Environmental Research. 2006; 62: S29–S33.
   PubMed Web of Science ®Google Scholar
• Sanchez W., Palluel O., Meunier L., Coquery M., Porcher J.-M., Aït-Aïssa S. Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environmental Toxicology and Pharmacology. 2005; 19: 177–183.
   PubMed Web of Science ®Google Scholar
• Schmidt H., Bernet D., Wahli T., Meier W., Burkhardt-Holm P. Active biomonitoring with brown trout and rainbow trout in diluted sewage plant effluents. Journal of Fish Biology. 1999; 54: 585–596.
   Web of Science ®Google Scholar
• Schmidt-Posthaus H., Bernet D., Wahli T., Burkhardt-Holm P. Morphological organ alterations and infectious diseases in brown trout Salmo trutta and rainbow trout Oncorhynchus mykiss exposed to polluted river water. Diseases of Aquatic Organisms. 2001; 44: 161–170.
   PubMed Web of Science ®Google Scholar
• Schwaiger J. Histopathological alterations and parasite infection in fish: indicators of multiple stress factors. Journal of Aquatic Ecosystem Stress and Recovery. 2001; 8: 231–240.
   Google Scholar
• Schwaiger J., Wanke R, Adam S., Pawert M., Honnen W., Triebskorn R. The use of histopathological indicators to evaluate contaminant-related stress in fish. Journal of Aquatic Ecosystem Stress and Recovery. 1997; 6: 75–85.
   Google Scholar
• Schwindt A.R., Truelove N., Schreck C.B., Fournie J.W., Landers D.H., Kent M.L. Quantitative evaluation of macrophage aggregates in brook trout Salvelinus fontinalis and rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms. 2006; 68: 101–113.
   PubMed Web of Science ®Google Scholar
• Vandeputte C., Guizon I., Genestie-Denis I., Vannier B., Lorenzon G. A microtiter plate assay for total glutathione and glutathione disulfide contents in cultured/isolated cells: performance study of a new miniaturized protocol. Cell Biology and Toxicology. 1994; 10: 415–421.
   PubMed Web of Science ®Google Scholar
• Van der Oost R., Beyer J., Vermeulen N.P.E. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology. 2003; 13: 57–149.
   PubMed Web of Science ®Google Scholar
• Wilhelm Filho D., Torres M.A., Tribess T.B., Pedrosa R.C., Soares C.H.L. Influence of season and pollution on the antioxidant defenses of the cichlid fish acara (Geophagus brasiliensis). Brazilian Journal of Medical and Biological Research. 2001; 34: 719–726.
   Web of Science ®Google Scholar