Vet Med - Czech, 2016, 61(1):35-50 | DOI: 10.17221/8681-VETMED

Biochemical, haematological and oxidative stress responses of common carp (Cyprinus carpio L.) after sub-chronic exposure to copperOriginal Paper

M. Sevcikova1, H. Modra1, J. Blahova1, R. Dobsikova1, L. Plhalova1, O. Zitka2, D. Hynek2, R. Kizek2, M. Skoric1, Z. Svobodova1
1 University of Veterinary and Pharmaceutical Sciences, Brno, Czech Republic
2 Mendel University, Brno, Czech Republic

The aim of the present study was to investigate the impact of copper-based pesticides (at concentrations of copper of 20, 30, 40 and 70 µg/l) on one-year-old common carp (Cyprinus carpio L.) during 28 days of exposure. Abnormal behaviour was observed in fish exposed to 70 µg/lfrom Day14. Histological alterations were noticed only in liver in the groups exposed to 40 and 70 µg/l.Significant changes (P ˂ 0.05) in almost all haematological indices were found, especially in the group exposed to the highest concentration of copper (70 µg/l). Biochemical analysis revealed various significant (P ˂ 0.05) differences among the tested groups. Significant differences in copper tissue concentration (P ˂ 0.05) among groups were found in liver, gills and kidney. Among antioxidative enzymes, significant changes were revealed mainly in catalase and glutathione-S-transferase activity (P ˂ 0.05). In gills, metallothionein content increased significantly (P ˂ 0.05) in the group exposed to the highest copper concentration (70 µg/l) compared with the other tested groups, including the control. A significant (P ˂ 0.05) change in total glutathione content was recorded in liver and gills, although the reduced/oxidised ratio was not affected. Oxidative damage to lipids increased significantly (P ˂ 0.05) with increasing copper concentration in liver and kidney. The results demonstrate the deleterious influence of copper on common carp even at low, environmentally relevant concentrations.

Keywords: metals; fish; antioxidant defence; pesticides

Published: January 31, 2016  Show citation

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Sevcikova M, Modra H, Blahova J, Dobsikova R, Plhalova L, Zitka O, et al.. Biochemical, haematological and oxidative stress responses of common carp (Cyprinus carpio L.) after sub-chronic exposure to copper. Vet Med - Czech. 2016;61(1):35-50. doi: 10.17221/8681-VETMED.
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    References

    1. Abdel-Tawwab M, Mousa MAA, Ahmad MH, Sakr SFM (2007): The use of calcium pre-exposure as a protective agent against environmental copper toxicity for juvenile Nile tilapia, Oreochromis niloticus (L.). Aquaculture 264, 236-246. Go to original source...
    2. Aebi H (1984): Catalase in vitro. Methods in Enzymology 105, 121-126. Go to original source... Go to PubMed...
    3. Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000): Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochimica et Biophysica Acta-General Subjects 1523, 37-48. Go to original source... Go to PubMed...
    4. Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006): Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquatic Toxicology 76, 160-202. Go to original source... Go to PubMed...
    5. An YJ, Kampbell DH (2003): Total, dissolved, and bioavailable metals at Lake Texoma marinas. Environmental Pollution 122, 253-259. Go to original source... Go to PubMed...
    6. Bennani N, Schmid Alliana A, Lafaurie M (1996): Immunotoxic effects of copper and cadmium in the sea bass Dicentrarchus labrax. Immunopharmacology and Immunotoxicology 18, 129-144. Go to original source... Go to PubMed...
    7. Benzie IFF, Strain JJ (1996): The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": The FRAP assay. Analytical Biochemistry 239, 70-76. Go to original source... Go to PubMed...
    8. Bervoets L, Blust R (2003): Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environmental Pollution 126, 9-19. Go to original source... Go to PubMed...
    9. Borvinskaya EV, Smirnov LP, Nemova NN (2013): An alpha class glutathione S-transferase from pike liver. Russian Journal of Bioorganic Chemistry 39, 498-503. Go to original source...
    10. Carlberg I, Mannervik B (1975): Purification and characterization of flavoenzyme glutathione reductase from rat liver. Journal of Biological Chemistry 250, 5475-5480. Go to original source...
    11. Carvalho CS, Fernandes MN (2006): Effect of temperature on copper toxicity and hematological responses in the neotropical fish Prochilodus scrofa at low and high pH. Aquaculture 251, 109-117. Go to original source...
    12. Cazenave J, Wunderlin DA, Hued AC, Bistoni MDA (2005): Haematological parameters in a neotropical fish, Corydoras paleatus (Jenyns, 1842) (Pisces, Callichthyidae), captured from pristine and polluted water. Hydrobiologia 537, 25-33. Go to original source...
    13. Celechovska O, Svobodova Z, Zlabek V, Macharackova B (2007): Distribution of metals in tissues of the common carp (Cyprinus carpio L.). Acta Veterinaria Brno 76, S93- S100. Go to original source...
    14. Ceron JJ, Martinez-Subiela S (2004): An automated spectrophotometric method for measuring canine ceruloplasmin in serum. Veterinary Research 35, 671-679. Go to original source... Go to PubMed...
    15. Cho YS, Lee SY, Kim KY, Bang IC, Kim DS, Nam YK (2008): Gene structure and expression of metallothionein during metal exposures in Hemibarbus mylodon. Ecotoxicology and Environmental Safety 71, 125-137. Go to original source... Go to PubMed...
    16. Clark MS, Bendell L, Power DM, Warner S, Elgar G, Ingleton PM (2002): Calcitonin: characterisation and expression in a teleost fish, Fugu rubripes. Journal of Molecular Endocrinology 28, 111-123. Go to original source... Go to PubMed...
    17. Dabrowski K, Lee KJ, Guz L, Verlhac V, Gabaudan J (2004): Effects of dietary ascorbic acid on oxygen stress (hypoxia or hyperoxia), growth and tissue vitamin concentrations in juvenile rainbow trout (Oncorhynchus mykiss). Aquaculture 233, 383-392. Go to original source...
    18. Dautremepuits C, Betoulle S, Vernet G (2002): Antioxidant response modulated by copper in healthy or parasitized carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Biochimica et Biophysica Acta-General Subjects 1573, 4-8. Go to original source... Go to PubMed...
    19. De Boeck G, De Smet H, Blust R (1995): The effect of sublethal levels of copper on oxygen-consumption and ammonia excretion in the common carp, Cyprinus carpio. Aquatic Toxicology 32, 127-141. Go to original source...
    20. De Boeck G, Vlaeminck A, Blust R (1997): Effects of sublethal copper exposure on copper accumulation, food consumption, growth, energy stores, and nucleic acid content in common carp. Archives of Environmental Contamination and Toxicology 33, 415-422. Go to original source... Go to PubMed...
    21. De Boeck G, Vlaeminck A, Balm PHM, Lock RAC, De Wachter B, Blust R (2001): Morphological and metabolic changes in common carp, Cyprinus carpio, during shortterm copper exposure: Interactions between Cu2+ and plasma cortisol elevation. Environmental Toxicology and Chemistry 20, 374-381. Go to original source... Go to PubMed...
    22. De Boeck G, Ngo TTH, Van Campenhout K, Blust R (2003): Differential metallothionein induction patterns in three freshwater fish during sublethal copper exposure. Aquatic Toxicology 65, 413-424. Go to original source... Go to PubMed...
    23. De Boeck G, Meeus W, De Coen W, Blust R (2004): Tissuespecific Cu bioaccumulation patterns and differences in sensitivity to waterborne Cu in three freshwater fish: rainbow trout (Oncorhynchus mykiss), common carp (Cyprinus carpio), and gibel carp (Carassius auratus gibelio). Aquatic Toxicology 70, 179-188. Go to original source... Go to PubMed...
    24. De Lafontaine Y, Gagne F, Blaise C, Costan G, Gagnon P, Chan HM (2000): Biomarkers in zebra mussels (Dreissena polymorpha) for the assessment and monitoring of water quality of the St Lawrence River (Canada). Aquatic Toxicology 50, 51-71. Go to original source... Go to PubMed...
    25. Dethloff GM, Bailey HC (1998): Effects of copper on immune system parameters of rainbow trout (Oncorhynchus mykiss). Environmental Toxicology and Chemistry 17, 1807-1814. Go to original source...
    26. Di Giulio RT, Meyer JN (2008): Reactive oxygen species and oxidative stress. In: Di Giulio RT, Hinton DE (eds.): The Toxicology of Fishes. 1st ed. CRC Press, 273-325. Go to original source...
    27. Eyckmans M, Celis N, Horemans N, Blust R, De Boeck G (2011): Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquatic Toxicology 103, 112-120. Go to original source... Go to PubMed...
    28. Fabrik I, Ruferova Z, Hilscherova K, Adam V, Trnkova L, Kizek R (2008): A determination of metallothionein in larvae of freshwater midges (Chironomus riparius) using Brdicka reaction. Sensors 8, 4081-4094. Go to original source... Go to PubMed...
    29. Flohe L, Gunzler WA (1984): Assays of glutathione peroxidase. Methods in Enzymology 105, 114-121. Go to original source... Go to PubMed...
    30. Gill TS, Tewari H, Pande J (1992): Short-term and long-term effects of copper on the rosy barb (Puntius conchicus Ham). Ecotoxicology and Environmental Safety 23, 294-306. Go to original source... Go to PubMed...
    31. Grosell M (2012): Copper. In: Wood CM, Farrell AP, Brauner CJ (eds.): Homeostasis and Toxicology of Essential Metals. 1st ed. Academic Press, Elsevier. 53-134. Go to original source...
    32. Grosell M, Marshall WS (2006): Ion transport, osmoregulation, and acid-base balance. In: Evans DH, Claiborne JB (eds.): The Physiology of Fishies. CRC Press, Taylor & Francis. 177-230.
    33. Grosell M, Hogstrand C, Wood CM (1998): Renal Cu and Na excretion and hepatic Cu metabolism in both Cu acclimated and non acclimated rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 40, 275-291. Go to original source...
    34. Grosell M, Nielsen C, Bianchini A (2002): Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comparative Biochemistry and Physiology C - Toxicology and Pharmacology 133, 287-303. Go to original source... Go to PubMed...
    35. Habig WH, Pabst MJ, Jakoby WB (1974): Glutathione S-transferases - first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry 249, 7130-7139. Go to original source...
    36. Haluzova I, Modra H, Blahova J, Marsalek P, Siroka Z, Groch L, Svobodova Z (2010): Effects of subchronic exposure to Spartakus (prochloraz) on common carp Cyprinus carpio. Neuroendocrinology Letters 31, 105-113. Go to PubMed...
    37. Hansen BH, Romma S, Garmo OA, Olsvik PA, Andersen RA (2006): Antioxidative stress proteins and their gene expression in brown trout (Salmo trutta) from three rivers with different heavy metal levels. Comparative Biochemistry and Physiology C - Toxicology and Pharmacology 143, 263-274. Go to original source... Go to PubMed...
    38. Harris ED (1991): Copper transport - an overview. Experimental Biology and Medicine 196, 130-140. Go to original source... Go to PubMed...
    39. Hassaan MS, Goda AM, Mahmoud SA, Tayel SI (2014): Protective effect of dietary vitamin E against fungicide copperoxychloride stress on Nile tilapia, Oreochromis niloticus (L.) fingerlings. International Aquatic Research 6, 1-7. Go to original source...
    40. Hernandez PP, Moreno V, Olivari FA, Allende ML (2006): Sub-lethal concentrations of waterborne copper are toxic to lateral line neuromasts in zebrafish (Danio rerio). Hearing Research 213, 1-10. Go to original source... Go to PubMed...
    41. Heydarnejad MS, Khosravian-Hemami M, Nematollahi A, Rahnama S (2013): Effects of copper at sublethal concentrations on growth and biochemical parameters in rainbow trout (Oncorhynchus mykiss). International Review of Hydrobiology 98, 71-79. Go to original source...
    42. Jebali J, Banni M, Gerbej H, Boussetta H, Lopez-Barea J, Alhama J (2008): Metallothionein induction by Cu, Cd and Hg in Dicentrarchus labrax liver: Assessment by RPHPLC with fluorescence detection and spectrophotometry. Marine Environmental Research 65, 358-363. Go to original source... Go to PubMed...
    43. Jezierska B, Witeska M (2001): Metal Toxicity to Fish. 1st ed. University of Podlasie, Siedlce, Poland. 318 pp.
    44. Julliard AK, Saucier D, Astic L (1993): Effect of chronic low-level copper exposure on ultrastructure of the olfactory system in rainbow trout (Oncorhynchus mykiss). Histology and Histopathology 8, 655-672. Go to PubMed...
    45. Kamunde C, McPhail R (2008): Bioaccumulation and hepatic speciation of copper in rainbow trout (Oncorhynchus mykiss) during chronic waterborne copper exposure. Archives of Environmental Contamination and Toxicology 54, 493-503. Go to original source... Go to PubMed...
    46. Kandemir S, Dogru MI, Orun I, Dogru A, Altas L, Erdogan K, Orun G, Polat N (2010): Determination of heavy metal levels, oxidative status, biochemical and hematological parameters in Cyprinus carpio L., 1758 from Bafra (Samsun) fish lakes. Journal of Animal and Veterinary Advances 9, 617-622. Go to original source...
    47. Karan V, Vitorovic S, Tutundzic V, Poleksic V (1998): Functional enzymes activity and gill histology of carp after copper sulfate exposure and recovery. Ecotoxicology and Environmental Safety 40, 49-55. Go to original source... Go to PubMed...
    48. Kawauchi H, Sower SA, Moriyama S (2009): The neuroendocrine regulation of prolactin and somatolactin secretion in fish. In: Barnier NJ, Van Der Kraak G, Farrell AP, Brauner CJ (eds.): Fish Endocrinology. 1st ed. Academic Press, Elsevier. 198-235. Go to original source...
    49. Kondera E, Witeska M (2013): Cadmium and copper reduce hematopoietic potential in common carp (Cyprinus carpio L.) head kidney. Fish Physiology and Biochemistry 39, 755-764. Go to original source... Go to PubMed...
    50. Kono Y, Fridovich I (1982): Superoxide radical inhibits catalase. Journal of Biological Chemistry 257, 5751-5754. Go to original source...
    51. Kretzschmar M (1996): Regulation of hepatic glutathione metabolism and its role in hepatotoxicity. Experimental and Toxicologic Pathology 48, 439-446. Go to original source... Go to PubMed...
    52. Kuzmina VV (2011): The influence of zinc and copper on the latency period for feeding and the food uptake in common carp, Cyprinus carpio L. Aquatic Toxicology 102, 73-78. Go to original source... Go to PubMed...
    53. Leaver MJ, George SG (1998): A piscine glutathione Stransferase which efficiently conjugates the end-products of lipid peroxidation. Marine Environmental Research 46, 71-74. Go to original source...
    54. Lebrun JD, Uher E, Tusseau-Vuillemin MH, Gourlay-France C (2014): Essential metal contents in indigenous gammarids related to exposure levels at the river basin scale: Metal-dependent models of bioaccumulation and geochemical correlations. Science of the Total Environment 466-467, 100-108. Go to original source... Go to PubMed...
    55. Lushchak VI (2011): Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology 101, 13-30. Go to original source... Go to PubMed...
    56. Lushchak VI, Bagnyukova TV, Husak VV, Luzhna LI, Lushchak OV, Storey KB (2005): Hyperoxia results in transient oxidative stress and an adaptive response by antioxidant enzymes in goldfish tissues. International Journal of Biochemistry and Cell Biology 37, 1670-1680. Go to original source... Go to PubMed...
    57. Luza SC, Speisky HC (1996): Liver copper storage and transport during development: implications for cytotoxicity. The American Journal of Clinical Nutrition 63, 812S-820S. Go to original source... Go to PubMed...
    58. Mansour SA, Sidky MM (2002): Ecotoxicological studies. 3. Heavy metals contaminating water and fish from Fayoum Governorate, Egypt. Food Chemistry 78, 15-22. Go to original source...
    59. Maracine M, Segner H (1998): Cytotoxicity of metals in isolated fish cells: Importance of the cellular glutathione status. Comparative Biochemistry and Physiology A - Molecular and Integrative Physiology 120, 83-88. Go to original source...
    60. Mikulikova I, Modra H, Blahova J, Marsalek P, Groch L, Siroka Z, Kruzikova K, Jarkovsky J, Littnerova S, Svobodova Z (2011): The effects of Click 500 SC (terbuthylazine) on common carp Cyprinus carpio under (sub)chronic conditions. Neuroendocrinology Letters 32, 15-24. Go to PubMed...
    61. Moon TW (2001): Glucose intolerance in teleost fish: face or fiction? Comparative Biochemistry and Physiology B - Biochemistry and Molecular Biology 129, 243-249. Go to original source... Go to PubMed...
    62. Muhvich AG, Jones RT, Kane AS, Anderson RS, Reimscheussel R (1995): Effects of chronic copper exposure on the macrophage chemiluminiscent response and gills histology in goldfish (Carassius auratus L.). Fish and Shellfish Immunology 5, 251-264. Go to original source...
    63. Nespolo RF, Rosenmann M (2002): Intraspecific allometry of haematological parameters in Basilichthys australis. Journal of Fish Biology 60, 1358-1362. Go to original source...
    64. Oliva M, Vicente JJ, Gravato C, Guilhermino L, GalindoRiano MD (2012): Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): Seasonal and spatial variation. Ecotoxicology and Environmental Safety 75, 151-162. Go to original source... Go to PubMed...
    65. Pandey S, Ahmad I, Parvez S, Bin-Hafeez B, Haque R, Raisuddin S (2001): Effect of endosulfan on antioxidants of freshwater fish Channa punctatus Bloch: 1. Protection against lipid peroxidation in liver by copper preexposure. Archives of Environmental Contamination and Toxicology 41, 345-352. Go to original source... Go to PubMed...
    66. Parvez S, Raisuddin S (2006): Copper modulates non-enzymatic antioxidants in the freshwater fish Channa punctata (Bloch) exposed to deltamethrin. Chemosphere 62, 1324-1332. Go to original source... Go to PubMed...
    67. Parvez S, Sayeed I, Pandey S, Ahmad A, Bin-Hafeez B, Haque R, Ahmad I, Raisuddin S (2003): Modulatory effect of copper on nonenzymatic antioxidants in freshwater fish Channa punctatus (Bloch.). Biological Trace Element Research 93, 237-248. Go to original source... Go to PubMed...
    68. Pelgrom S, Lock RAC, Balm PHM, Bonga SEW (1995): Integrated physiological response of tilapia, Oreochromis mossambicus, to sublethal copper exposure. Aquatic Toxicology 32, 303-320. Go to original source...
    69. Perumalsamy N, Arumugam K (2013): Enzymes activity in fish exposed to heavy metals and the electro-plating effluent at sub-lethal concentrations. Water Quality Exposure and Health 5, 93-101. Go to original source...
    70. Pretto A, Loro VL, Silva VMM, Salbego J, De Menezes CC, Souza CD, Gioda CR, Baldisserotto B (2014): Exposure to sublethal concentrations of copper changes biochemistry parameters in silver catfish, Rhamdia quelen, Quoy and Gaimard. Bulletin of Environmental Contamination and Toxicology 92, 399-403. Go to original source... Go to PubMed...
    71. Pyle GG, Mirza RS (2007): Copper-impaired chemosensory function and behavior in aquatic animals. Human and Ecological Risk Assessment 13, 492-505. Go to original source...
    72. Roesijadi G (1996): Metallothionein and its role in toxic metal regulation. Comparative Biochemistry and Physiology C - Toxicology and Pharmacology 113, 117-123. Go to original source...
    73. Rougier F, Troutaud D, Ndoye A, Deschaux P (1994): Nonspecific immune response of Zebrafish, Brachydanio rerio (Hamilton-Buchanan) following copper and zinc exposure. Fish and Shellfish Immunology 4, 115-127. Go to original source...
    74. Ruas CBG, Carvalho CD, De Araujo HSS, Espindola ELG, Fernandes MN (2008): Oxidative stress biomarkers of exposure in the blood of cichlid species from a metalcontaminated river. Ecotoxicology and Environmental Safety 71, 86-93. Go to original source... Go to PubMed...
    75. Sanchez W, Palluel O, Meunier L, Coquery M, Porcher JM, Ait-Aissa S (2005): Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environmental Toxicology and Pharmacology 19, 177-183. Go to original source... Go to PubMed...
    76. Shukla N, Maher J, Masters J, D Angelini G, Jeremy JY (2006): Does oxidative stress change ceruloplasmin from a protective to a vasculopathic factor? Atherosclerosis 187, 238-250. Go to original source... Go to PubMed...
    77. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985): Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150, 76-85. Go to original source... Go to PubMed...
    78. Stohs SJ, Bagchi D (1995): Oxidative mechanisms in the toxicity of metal-ions. Free Radical Biology and Medicine 18, 321-336. Go to original source... Go to PubMed...
    79. Svobodova Z, Vykusova B, Machova J (1994): The effects of pollutants on selected haematological and biochemical parameters in fish. In: Muller R, Lloyd R (eds.): Sublethal and Chronic Effects of Pollutants on Freshwater Fish, FAO Fishing News Books, 39-52.
    80. Svobodova Z, Pravda D, Modra H (2012): Methods of haematological examination of fish (in Czech). University of South Bohemia in Ceske Budejovice, Faculty of Fisheries and Protection of Waters, Czech Republic, 38 pp.
    81. Takei Y, Loretz CA (2006): Endocrinology. In: Evans DH, Claiborne JB (eds.): The Physiology of Fishes. 3rd ed. CRC Press, Taylor & Francis. 272-342.
    82. Tang QQ, Feng L, Jiang WD, Liu Y, Jiang J, Li SH, Kuang SY, Tang L, Zhou XQ (2013): Effects of dietary copper on growth, digestive, and brush border enzyme activities and antioxidant defense of hepatopancreas and intestine for young grass carp (Ctenopharyngodon idella). Biological Trace Element Research 155, 370-380. Go to original source... Go to PubMed...
    83. Teodorescu D, Munteanu MC, Staicu AC, Dinischiotu A (2012): Changes in lactate dehydrogenase activity in Carassius auratus gibelio (L. Pysces) kidney, gills and intestine induced by acute exposure to copper. Romanian Biotechnological Letters 17, 7873-7880.
    84. Van der Oost R, Beyer J, Vermeulen NPE (2003): Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology 13, 57-149. Go to original source... Go to PubMed...
    85. Van Vuren JHJ, Van Der Merwe M, Du Preez HH (1994): The effect of copper on the blood chemistry of Clarias gariepinus (Clariidae). Ecotoxicology and Environmental Safety 29, 187-199. Go to original source... Go to PubMed...
    86. Varanka Z, Rojik I, Varanka I, Nemcsok J, Abraham M (2001): Biochemical and morphological changes in carp (Cyprinus carpio L.) liver following exposure to copper sulfate and tannic acid. Comparative Biochemistry and Physiology C - Toxicology and Pharmacology 128, 467-478. Go to original source... Go to PubMed...
    87. Vutukuru SS, Chintada S, Madhavi KR, Rao JV, Anjaneyulu Y (2006): Acute effects of copper on superoxide dismutase, catalase and lipid peroxidation in the freshwater teleost fish, Esomus danricus. Fish Physiology and Biochemistry 32, 221-229. Go to original source...
    88. Wang CL, Zhang FT, Cao WX, Wang JW (2014): The identification of metallothionein in rare minnow (Gobiocypris rarus) and its expression following heavy metal exposure. Environmental Toxicology and Pharmacology 37, 1283-1291. Go to original source... Go to PubMed...
    89. WHO (1998): Environmental Health Criteria 200: Copper, Geneva, Switzerland.
    90. Wilson RW, Wright PM, Munger S, Wood CM (1994): Ammonia excretion in freshwater rainbow trout (Oncorhynchus mykiss) and the importance of gill boundary layer acidification: lack of evidence for Na+/NH4+ exchange. Journal of Experimental Biology 191, 37-58. Go to original source... Go to PubMed...
    91. Witeska M, Kondera E, Lipionoga J, Nienaltowska R (2009): The changes in blood leukocyte profile of common carp induced by acute exposures to copper and cadmium. Fresenius Environmental Bulletin 18, 1534-1540.
    92. Witeska M, Kondera E, Lipionoga J, Jastrzebska A (2010): Changes in oxygen consumption rate and red blood parameters in common carp Cyprinus carpio L. after acute copper and cadmium exposures. Fresenius Environmental Bulletin 19, 115-122.

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