Abstract
The toxicity of copper (Cu) on growth and activities of digestive and antioxidant enzymes in the hepatopancreas and intestine of juvenile Qihe crucian carp Carassius carassius was evaluated. The fish were exposed in different Cu solutions for 20 days, and the 0.60 mg/L group was then transferred to clean water to initiate a 20-day recovery period after Cu exposure. Results showed that all enzyme activities decreased significantly at high-concentration (0.30 and 0.60 mg/L) and long-time (20 days) Cu exposures and increased significantly at high-concentration (0.60 mg/L) and short-time Cu exposures (1 day). After the 20-day recovery period, all enzyme activities in the 0.60 mg/L group had recovered to control levels. High-concentration (0.60 mg/L) and long-time (20 days) Cu exposure markedly hindered the growth of fish, whereas the loss of fish growth can not be compensated for by a 20-day recovery period.
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Azeez A, Sane AP, Bhatnagar D, Nath P (2007) Enhanced expression of serine proteases during floral senescence in Gladiolus. Phytochemistry 68:1352–1357
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248
Cakmak I, Strbac D, Marschner H (1993) Activities of hydrogen peroxide-scavenging enzymes in germinating wheat seeds. J Exp Bot 44:127–132
Cengiz EI, Unlu E (2006) Sublethal effects of commercial deltamethrin on the structure of the gill, liver and gut tissues of mosquitofish, Gambusia affinis: a microscopic study. Environ Toxicol Phanmacol 21:246–253
Chien YH, Pan CH, Hunter H (2003) The resistance to physical stresses by Penaeus monodon juveniles fed diets supplemented with astaxanthin. Aquaculture 216:177–191
Das PC, Ayyappan S, Jena JK, Das BK (2004) Acute toxicity of ammonia and its sub-lethal effects on selected haematological and enzymatic parameters of mrigal, Cirrhinus mrigala (Hamilton). Aquac Res 35:134–143
Dedourge-Geffard O, Palais F, Biagianti-Risbourg S, Geffard O, Geffard A (2009) Effects of metals on feeding rate and digestive enzymes in Gammarus fossarum: an in situ experiment. Chemosphere 77:1569–1576
GB (1989) Water quality standard for fisheries of the State Standard of the People’s Republic of China: GB11607–89. Ministry of Environmental Protection of the People’s Republic of China, Beijing, China (in Chinese)
Hansen JA, Lipton J, Welsh PG, Morris J, Cacela D, Suedkamp MJ (2002) Relationship between exposure duration, tissue residues, growth, and mortality in rainbow trout (Oncorhynchus mykiss) juveniles sub-chronically exposed to copper. Aquat Toxicol 58:175–188
James R, Sampath K, Jothilakshmi S, Vasudhevan I, Thangarathinam R (2008) Effects of copper toxicity on growth, reproduction and metal accumulation in chosen ornamental fishes. Ecohydrol Hydrobiol 8(1):89–97
Jiang HX, Yang HM, Kong XH, Wang SP, Liu DQ, Shi SJ (2012) Response of acid and alkaline phosphatase activities to copper exposure and recovery in freshwater fish Carassius auratus gibelio var. Life Sci J 9(3):233–245
Jiang WD, Liu Y, Hua K, Jiang J, Li SH, Feng L, Zhou XQ (2014) Copper exposure induces oxidative injury, disturbs the antioxidant system and changes the Nrf2/ARE (CuZnSOD) signaling in the fish brain: protective effects of myo-inositol. Aquat Toxicol 155:301–313
Kong XH, Jiang HX, Wang SP, Wu XM, Fei W, Li L, Nie GX, Li XJ (2013) Effects of copper exposure on the hatching status and antioxidant defense at different developmental stages of embryos and larvae of goldfish Carassius auratus. Chemosphere 92:1458–1464
Kuz’mina VV, Ushakova NV (2010) The dependence on temperature and pH of the effects of zinc and copper on proteolytic activities of the digestive tract mucosa in piscivorous fish and their potential preys. Fish Physiol Biochem 36:787–795
Li LJ, Liu XM, Guo YP, Ma EB (2005) Activity of the enzymes of the antioxidative system in cadmium-treated Oxya chinensis (Orthoptera Acridoidae). Environ Toxicol Pharmacol 20:412–416
Li JS, Li JL, Wu TT (2007) The effects of copper, iron and zinc on digestive enzyme activity in the hybrid tilapia Oreochromis niloticus (L.) × Oreochromis aureus (Steindachner). J Fish Biol 71:1788–1798
Li N, Zhao YL, Yang J (2008) Effects of water-borne copper on digestive and metabolic enzymes of the giant freshwater prawn Macrobrachium rosenbergii. Arch Environ Contam Toxicol 55:86–93
Liu C, Fu JX, Xue F, Zhao YH, Zhu ZF (2007) Experimental studies on the influencing factors of algae killing by copper sulfate. Contemp Chem Ind 5:488–491 (in Chinese)
Liu XJ, Luo Z, Xiong BX, Liu X, Zhao YH, Hu GF, Lv GJ (2010) Effect of waterborne copper exposure on growth, hepatic enzymatic activities and histology in Synechogobius hasta. Ecotoxicol Environ Saf 73:1286–1291
Mastin BJ, Rodgers JH (2000) Toxicity and bioavailability of copper herbicides (Clearigate, Cutrine-Plus, and copper sulfate) to freshwater animals. Arch Environ Contam Toxicol 39:445–451
Muhlia-Almazán A, García-Carreño FL (2002) Influence of molting and starvation on the synthesis of proteolytic enzymes in the midgut gland of the white shrimp Penaeus vannamei. Comp Biochem Physiol 133:383–394
Orbea A, Ortiz-Zarragoitia M, Solé M, Porte C, Cajaraville MP (2002) Antioxidant enzymes and peroxisome proliferation in relation to contaminant body burdens of PAHs and PCBs in bivalve molluscs, crabs and fish from the Urdaibai and Plentzia estuaries (Bay of Biscay). Aquat Toxicol 58:75–98
Oruc EO, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Physiol 137C:43–51
Rick W, Stegbauer HP (1984) Alfa-amylase. In: Bergmeyer HU, Grab M (eds) Methods of enzymatic analysis. Enzymes, vol 5. Academic Press, New York, pp 885–889
Ross SW, Dalton DA, Kranmer S, Christensen BL (2001) Physiological (antioxidant) responses of estuarine fishes to variability in dissolved oxygen. Comp Biochem Physiol 130C:289–303
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). Biol Trace Elem Res 155:370–380
Tsuzuki MY, Sugai JK, Maciel JC, Francisco CJ, Cerqueira VR (2007) Survival, growth and digestive enzyme activity of juveniles of the fat snook (Centropomus parallelus) reared at different salinities. Aquaculture 271:319–325
Von Borell E (2000) Stress and coping in farm animals. Arch Tierz (Sonderheft) 43:144–152
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 Physiol Biochem 32:221–229
Wang L, Yan B, Liu N, Li Y, Wang Q (2008) Effects of cadmium on glutathione synthesis in hepatopancreas of freshwater crab, Sinopotamon yangtsekiense. Chemosphere 74:51–56
Wang T, Long XH, Cheng YZ, Liu ZP, Yan SH (2015) A comparison effect of copper nanoparticles versus copper sulphate on juvenile Epinephelus coioides: growth parameters, digestive enzymes, body composition, and histology as biomarkers. Int J Genomics 14:1–10
Ye JS, Chen XJ, Zhu YY (2013) Influence of pH on survival, growth and activities of digestive enzymes of Odontobutis obscures. Adv J Food Sci Technol 5:1234–1237
Zhang JJ, Yang XB (2012) Fishery water quality evaluation of Qihe crucian carp national aquatic germplasm resources conservation area in Henan province. Henan Fish 1:40–42 (in Chinese)
Zhang JF, Shen H, Xu TL, Wang XR, Li WM, Gu YF (2003) Effects of long-term exposure of low-level diesel oil on the antioxidant defense system of fish. Bull Environ Contam Toxicol 71:234–239
Zhang JF, Shen H, Wang XR, Wu JC, Xue YQ (2004) Effects of chronic exposure of 2,4-dichlorophenol on the antioxidant system in liver of fresh water fish Carassius auratus. Chemosphere 55:167–174
Zhao HL, Xiao TY (2007) The resources status and protection countermeasures of Qihe crucian carp. Henan Fish 3:5–6 (in Chinese)
Acknowledgments
This work was sponsored by the Program for Science and Technology Innovation Talents in Universities of Henan Province (Grant No. 2011HASTIT012) and the Key Projects of Science and Technology Research of the Department of Education in Henan Province (Grant No. 13A240509). This study was also partly supported by the Key Subjects of Fisheries in Henan Province, China.
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Jiang, H., Kong, X., Wang, S. et al. Effect of Copper on Growth, Digestive and Antioxidant Enzyme Activities of Juvenile Qihe Crucian Carp, Carassius carassius, During Exposure and Recovery. Bull Environ Contam Toxicol 96, 333–340 (2016). https://doi.org/10.1007/s00128-016-1738-2
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DOI: https://doi.org/10.1007/s00128-016-1738-2