Waterborne copper sulfate toxicity in Nile tilapia (Oreochromis niloticus) juveniles affect survival, growth, and physiology

References

• Abdel-Baki, A. S., M. A. Dkhil, and S. Al-Quraishy. 2010. Bioaccumulation of some heavy metals in tilapia fish relevant to their concentration in water and sediment of Wadi Hanifah, Saudi Arabia. African Journal of Biotechnology 9:1658–62. doi:10.5897/AJB10.1772.
   Google Scholar
• Ahmed, M. K., M. Habibullah-Al-Mamun, E. Parvin, M. S. Akter, and M. S. Khan. 2013. Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, tilapia (Oreochromis mossambicus). Experimental and Toxicologic Pathology 65 (6):903–09. doi:10.1016/j.etp.2013.01.003.
   PubMedGoogle Scholar
• Al-Bairuty, G. A., B. J. Shaw, R. D. Handy, and T. B. Henry. 2013. Histopathological effects of waterborne copper nanoparticles and copper sulphate on the organs of rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 126:104–15. doi:10.1016/j.aquatox.2012.10.005.
   PubMed Web of Science ®Google Scholar
• Albinati, A. C. L., P. C. Soares, R. C. B. Albinati, E. L. T. Moreira, A. D. Lira, and J. V. CArvalho. 2017. Toxicidade do inseticida Tiametoxam para o Pacamã(Lophisiolurus alexandri). Pesquisa Veterinária Brasileira 37 (4):307–12. doi:10.1590/S0100-736X2017000400002.
   Google Scholar
• Ali, A., S. M. Al-Ogaily, N. A. Al-Asgah, and J. Gropp. 2003. Effect of sublethal concentrations of copper on the growth performance of Oreochromis niloticus. Journal of Applied Ichthyology 19 (4):183–88. doi:10.1046/j.1439-0426.2003.00440.x.
   Web of Science ®Google Scholar
• Alkobaby, A. I., and R. K. Abd El Wahed. 2017. The Acute toxicity of copper to Nile tilapia (Oreochromis niloticus) fingerlings and its effects on gill and liver histology. Journal of Aquaculture Research & Development 8 (1):1–6. doi:10.4172/2155-9546.1000465.
   Google Scholar
• Angeles-Escobar, B. E., S. M. B. C. da Silva, and W. Severi. 2021. Growth, red blood cells, and gill alterations of red pacu (Piaractus brachypomus) fingerlings by chronic exposure to different total suspended solids in biofloc. Journal of the World Aquaculture Society. doi:10.1111/jwas.12837.
   Web of Science ®Google Scholar
• Atli, G., and M. Canli. 2010. Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicology and Environmental Safety 73 (8):1884–89. doi:10.1016/j.ecoenv.2010.09.005.
   PubMed Web of Science ®Google Scholar
• Bost, M., S. Houdart, M. Oberli, E. Kalonji, J. F. Huneau, and I. Margaritis. 2016. Dietary copper and human health: Current evidence and unresolved issues. Journal of Trace Elements in Medicine and Biology 35:107–15. doi:10.1016/j.jtemb.2016.02.006.
   PubMed Web of Science ®Google Scholar
• Boyd, C. E. 1990. Water quality in ponds for aquaculture. Birmingham, Alabama, USA: Birmingham Publishing Co.
   Google Scholar
• Chen, W.-Y., C.-J. Lin, Y.-R. Ju, J.-W. Tsai, and C.-M. Liao. 2012. Assessing the effects of pulsed waterborne copper toxicity on life-stage tilapia populations. Science of the Total Environment 417-418:129–37. doi:10.1016/j.scitotenv.2011.12.043.
   PubMed Web of Science ®Google Scholar
• Chung, S., K. Ribeiro, J. F. B. Melo, D. V. Teixeira, L. V. O. Vidal, and C. E. Copatti. 2021a. Essential oil from ginger influences the growth, haematological and biochemical variables and histomorphometry of intestine and liver of Nile tilapia juveniles. Aquaculture 534:736325. doi:10.1016/j.aquaculture.2020.736325.
   Web of Science ®Google Scholar
• Chung, S., K. Ribeiro, D. V. Teixeira, and C. E. Copatti. 2021b. Inclusion of essential oil from ginger in the diet improves physiological parameters of tambaqui juveniles (Colossoma macropomum). Aquaculture 543:736934. doi:10.1016/j.aquaculture.2021.736934.
   Web of Science ®Google Scholar
• Collier, H. B. 1944. The standardizations of blood haemoglobin determination. Canadian Medical Association Journal 50 (6):550–52.
   PubMedGoogle Scholar
• Copatti, C. E., K. C. S. Bolner, E. P. Londero, F. L. De Rosso, M. A. Pavanato, and B. Baldisserotto. 2019. Low dissolved oxygen levels increase stress in piava (Megaleporinus obtusidens): Iono-regulatory, metabolic and oxidative responses. Anais da Academia Brasileira de Ciências 91 (3):e20180395. doi:10.1590/0001-3765201920180395.
   PubMed Web of Science ®Google Scholar
• Copatti, C. E., L. O. Garcia, and B. Baldisserotto. 2009. A revision about impact of agrochemicals used in the rice field in fishes. Biota Neotropica 9 (4):235–42. doi:10.1590/S1676-06032009000400023.
   Google Scholar
• Devi, Y., and A. Mishra. 2013. Histopathological alterations in gill and liver anotomy of fresh water, air breathing fish Channa Punctatus after pesticide Hilban® (Chlorpyrifos) Treatment. Advanced Biomedical Research 4:57–62.
   Google Scholar
• Eaton, A. D., L. S. Clesceri, E. W. Rice, and A. E. Greenberg. 2005. Standard methods for the examination of water and wastewater, 21 ed. Washington, DC: APHA.
   Google Scholar
• El-Bouhy, Z. M., R. M. Reda, and A. E. El-Azony. 2016. Effect of copper and lead as water pollutants on ectoparasitic infested Oreochromis niloticus. Zagazig Veterinary Journal 44 (2):156–66. doi:10.21608/ZVJZ.2016.7858.
   Google Scholar
• El-Keredy, M. S. A., A. M. El-Shenway, A. M. Diab, G. I. E. Ali, and W. S. Kotb. 2017. Effect of dietary vitamin C and В-Glucan to alleviate the toxic effect of copper sulphate in tilapia fish. Alexandria Journal of Veterinary Sciences 55 (1):36–49. doi:10.5455/ajvs.276295.
   Google Scholar
• El-Moselhy, K. M., L. I. Mohamedein, and M. A. Abdelmoneim. 2011. Acute toxicity of copper and mercury to different life stages of the Nile tilapia (Oreochromis niloticus). African Journal of Biological Sciences 7:13–21.
   Google Scholar
• Eroglu, A., Z. Dogan, E. G. Kanak, G. Atli, and M. Canli. 2015. Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism. Environmental Science and Pollution Research 22 (5):3229–37. doi:10.1007/s11356-014-2972-y.
   PubMed Web of Science ®Google Scholar
• FAO. 2020. The state of world fisheries and aquaculture 2020. Sustainability in action. Rome: Food and Agriculture Organization of the United Nations. doi:10.4060/ca9229en.
   Google Scholar
• Figueiredo-Fernandes, A., J. V. Ferreira-Cardoso, S. Garcia-Santos, S. M. Monteiro, J. Carrola, P. Matos, and A. Fontaínhas-Fernandes. 2007. Histopathological changes in liver and gill epithelium of Nile tilapia, Oreochromis niloticus, exposed to waterborne copper. Pesquisa Veterinária Brasileira 27 (3):103–09. doi:10.1590/S0100-736X2007000300004.
   Web of Science ®Google Scholar
• Fırat, Ö., H. Y. Cogun, T. A. Yüzereroğlu, G. Gök, Ö. Fırat, F. Kargin, and Y. Kötemen. 2011. A comparative study on the effects of a pesticide (cypermethrin) and two metals (copper, lead) to serum biochemistry of Nile tilapia, Oreochromis niloticus. Fish Physiology and Biochemistry 37 (3):657–66. doi:10.1007/s10695-011-9466-3.
   PubMed Web of Science ®Google Scholar
• Fuzinatto, C. F., L. Flohr, S. P. Melegari, and W. G. Matias. 2015. Oxidative stress and hypermethylation induced by exposure of Oreochromis niloticus to complex environmental mixtures of river water from Cubatão do Sul, Brazil. Ecotoxicology and Environmental Safety 114:190–97. doi:10.1016/j.ecoenv.2015.01.025.
   PubMed Web of Science ®Google Scholar
• Ghasemzadeh, A., and M. Bahrekazemi. 2019. The reduction of CuSO4 toxicity in common carp (Cyprinus carpio Linnaeus, 1758) after pre-exposure to CaCO3. The Asian Fisheries Science 32:11–116. doi:10.33997/j.afs.2019.32.3.003.
   Google Scholar
• Goldenfarb, P. B., F. P. Bowyer, E. Hall, and E. Brosious. 1971. Reproducibility in the hematology laboratory: The microhematocrit determinations. American Journal of Clinical Pathology 56 (1):35–39. doi:10.1093/ajcp/56.1.35.
   PubMed Web of Science ®Google Scholar
• Hassan, N. F., G. M. Soliman, E. F. Okasha, and A. M. Shalaby. 2018. Histological, immunohistochemical, and biochemical study of experimentally induced fatty liver in adult male albino rat and the possible protective role of pomegranate. Journal of Microscopy and Ultrastructure 6 (1):44–55. doi:10.4103/JMAU.JMAU_5_18.
   PubMedGoogle Scholar
• Hauser-Davis, R. A., R. T. Lavradas, R. C. Lavandier, E. G. A. Rojas, A. W. S. Guarino, and R. L. Ziolli. 2015. Accumulation and toxic effects of microcystin in tilapia (Oreochromis niloticus) from an eutrophic Brazilian lagoon. Ecotoxicology and Environmental Safety 112:132–36. doi:10.1016/j.ecoenv.2014.10.036.
   PubMed Web of Science ®Google Scholar
• Hoseini, S. M., H. Rajabiesterabadi, and S. Kordrostami. 2016. Chronic exposure of Rutilus rutilus caspicus fingerlings to ambient copper: Effects on food intake, growth performance, biochemistry and stress resistance. Toxicology and Industrial Health 32 (2):375–83. doi:10.1177/0748233713500825.
   PubMed Web of Science ®Google Scholar
• Javed, M., and N. Usmani. 2015. Impact of heavy metal toxicity on hematology and glycogen status of fish: A review. Proc. Natl. Acad. Sci. India Section B 85:889–900. doi:10.1007/s40011-014-0404-x.
   Google Scholar
• Javed, M., and N. Usmani. 2019. An overview of the adverse effects of heavy metal contamination on fish health. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences 89 (2):389–403. doi:10.1007/s40011-017-0875-7.
   Google Scholar
• Kanak, E. G., Z. Dogan, A. Eroglu, G. Atli, and M. Canli. 2014. Effects of fish size on the response of antioxidant systems of Oreochromis niloticus following metal exposures. Fish Physiology and Biochemistry 40 (4):1083–91. doi:10.1007/s10695-014-9907-x.
   PubMed Web of Science ®Google Scholar
• Kaya, H., M. Akbulut, E. Ş. Çelik, and S. Yılmaz. 2013. Impacts of sublethal lead exposure on the hemato-immunological parameters in tilapia (Oreochromis mossambicus). Toxicological & Environmental Chemistry 95 (9):1554–64. doi:10.1080/02772248.2014.895363.
   Web of Science ®Google Scholar
• Kondera, E., and M. Witeska. 2013. Cadmium and copper reduce hematopoietic potential in common carp (Cyprinus carpio L.) head kidney . Fish Physiology and Biochemistry 39 (4):755–64. doi:10.1007/s10695-012-9738-6.
   PubMed Web of Science ®Google Scholar
• Lemos, C. H. P., S. Chung, C. V. M. Ribeiro, and C. E. Copatti. 2018. Growth and biochemical variables in Amazon catfish (Pseudoplatystoma reticulatum♀ x Leiarius marmoratus♂) under different water pH. Anais da Academia Brasileira de Ciências 90 (4):3573–81. doi:10.1590/0001-3765201820180241.
   PubMed Web of Science ®Google Scholar
• Liu, X. J., Z. Luo, B. X. Xiong, X. Liu, Y. H. Zhao, G. F. Hu, and G. J. Lv. 2010. Effect of waterborne copper exposure on growth, hepatic enzymatic activities and histology in Synechogobius hasta. Ecotoxicology and Environmental Safety 73 (6):1286–91. doi:10.1016/j.ecoenv.2010.06.019.
   PubMed Web of Science ®Google Scholar
• Malhotra, N., T.-R. Ger, B. Uapipatanakul, J.-C. Huang, K. H.-C. Chen, and C.-D. Hsiao. 2020. Review of copper and copper nanoparticle toxicity in fish. Nanomaterials 10 (6):1126. doi:10.3390/nano10061126.
   Web of Science ®Google Scholar
• Mela, M., M. A. F. Randi, D. F. Ventura, C. E. V. Carvalho, E. Pelletier, and C. A. Oliveira Ribeiro. 2007. Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus. Ecotoxicology and Environmental Safety 68 (3):426–35. doi:10.1016/j.ecoenv.2006.11.013.
   PubMed Web of Science ®Google Scholar
• Meng, X.-L., S. Li, C.-B. Qin, Z.-X. Zhu, W.-P. Hu, L.-P. Yang, R.-H. Lu, W.-J. Li, and G.-X. Nie. 2018. Intestinal microbiota and lipid metabolism responses in the common carp (Cyprinus carpio L.) following copper exposure. Ecotoxicology and Environmental Safety 160:257–64. doi:10.1016/j.ecoenv.2018.05.050.
   PubMed Web of Science ®Google Scholar
• Mhuseen, H., and A. J. Mohammed. 2019. Heavy metals causing toxicity in fishes. Journal of Physics: Conference Series 1294 (6):062028. doi:10.1088/1742-6596/1294/6/062028.
   Google Scholar
• Moghimi, M., N. Mahboobi-Soofiani, and P. Malekpouri. 2018. Effects of water-borne copper and lead on metabolic and excretion rate of bahaii loach (Turcinoemacheilus bahaii). Environmental Toxicology and Pharmacology 60:176–83. doi:10.1016/j.etap.2018.04.023.
   PubMed Web of Science ®Google Scholar
• Monteiro, S. M., J. M. Mancera, A. Fontaínhas-Fernandes, and M. Sousa. 2005. Copper induced alterations of biochemical parameters in the gill and plasma of Oreochromis niloticus. Comparative Biochemistry and Physiology, Part C 141:375–83. doi:10.1016/j.cbpc.2005.08.002.
   PubMed Web of Science ®Google Scholar
• Morante, V. H. P., C. E. Copatti, A. R. L. Souza, M. M. Da Costa, L. G. T. Braga, A. M. Souza, F. V. S. T. Melo, A. C. S. Camargo, and F. B. M. Melo. 2021. Assessment the crude grape extract as feed additive for tambaqui (Colossoma macropomum), an omnivorous fish. Aquaculture 54:737068. doi:10.1016/j.aquaculture.2021.737068.
   Google Scholar
• Mutlu, E., S. Aydin, and B. Kutlu. 2015. Alterations of growth performance and blood chemistry in Nile tilapia (Oreochromis niloticus) affected by copper sulfate in long-term exposure. Turkish Journal of Fisheries and Aquatic Sciences 15 (2):487–93. doi:10.4194/1303-2712-v15_2_35.
   Google Scholar
• Naseem, A. R., A. Ullah, and J. Haider. 2015. Determination of acute toxicity of copper and cobalt for tilapia nilotica. Journal of Bioresource Management 2:16–25.
   Google Scholar
• Natt, M. P., and C. A. A. Herrick. 1952. New blood diluent for counting the erytrocytes and leucocites of chickens. Poultry Science 31 (4):182–88. doi:10.3382/ps.0310735.
   Web of Science ®Google Scholar
• Nitz, L. F., L. Pellegrin, D. S. B. Pinto, L. C. Maltez, C. E. Copatti, and L. Garcia. 2020. Secondary stress responses to hypoxia and re-oxygenation at different temperatures in pacu (Piaractus mesopotamicus) juveniles. Aquaculture Research 51 (11):4471–81. doi:10.1111/are.14792.
   Web of Science ®Google Scholar
• Nouh, W. G., and A. G. Selim. 2013. Toxopathological studies on the effect of formalin and copper sulphate in tilapia as a commonly used disinfectant in aquaculture. Journal of Applied Environmental and Biological Sciences 3:7–20.
   Google Scholar
• Omar, W. A., K. H. Zaghloul, A. A. Abdel-Khalek, and S. Abo-Hegab. 2013. Risk assessment and toxic effects of metal pollution in two cultured and wild fish species from highly degraded aquatic habitats. Archives of Environmental Contamination and Toxicology 65 (4):753–64. doi:10.1007/s00244-013-9935-z.
   PubMed Web of Science ®Google Scholar
• Pacheco, A. G., and M. F. Rebelo. 2013. A simple R-based function to estimate lethal concentrations. Marine Environmental Research 91:41–44. doi:10.1016/j.marenvres.2013.08.003.
   PubMed Web of Science ®Google Scholar
• Prophet, E. B., B. Mills, J. B. Arrington, and L. H. Sobin. 1992. Afip Laboratory methods in histotechnology. Washington, DC: American registry of pathology.
   Google Scholar
• Ranzani-Paiva, M. J. T., S. B. de Pádua, M. Tavares-Dias, and M. I. Egami. 2013. Métodos para análise hematológica em peixes. Maringá: EDUEM.
   Google Scholar
• R Development Core Team. 2015. R: A language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing, . http://www.R-project.org.
   Google Scholar
• Ribeiro, C. A. O., A. Katsumiti, P. França, J. Maschio, E. Zandoná, M. M. Cestari, T. Vicari, H. Roche, H. C. S. de Assis, and F. Filipak Neto. 2013. Biomarkers responses in fish (Atherinella brasiliensis) of Paranaguá Bay, Southern Brazil, for assessment of pollutant effects. Brazilian Journal of Oceanography 61 (1):1–11. doi:10.1590/S1679-87592013000100001.
   Web of Science ®Google Scholar
• Santos, C. R., A. L. M. Cavalcante, R. A. Hauser-Davis, R. M. Lopes, and R. D. C. O. Da Costa Mattos. 2016. Effects of sub-lethal and chronic lead concentrations on blood and liver ALA-D activity and hematological parameters in Nile tilapia. Ecotoxicology and Environmental Safety 129:250–56. doi:10.1016/j.ecoenv.2016.03.028.
   PubMed Web of Science ®Google Scholar
• Shaw, B. J., and R. D. Handy. 2011. Physiological effects of nanoparticles on fish: A comparison of nanometals versus metal ions. Environment International 37 (6):1083–97. doi:10.1016/j.envint.2011.03.009.
   PubMed Web of Science ®Google Scholar
• Shokr, E. A. M. 2020. Effect of copper on hematological, biochemical changes and reproductive hormones of the Nile tilapia Oreochromis niloticus. Egyptian Journal of Aquatic Biology and Fisheries 24 (2):1–18. doi:10.21608/ejabf.2020.76626.
   Google Scholar
• Singh, D., K. Nath, S. P. Trivedi, and Y. K. Sharma. 2008. Impact of copper on haematological profile of freshwater fish, Channa punctatus. Journal of Environmental Biology 29 (2):253–57.
   PubMed Web of Science ®Google Scholar
• Sonone, S. S., S. Jadhav, M. S. Sankhla, and R. Kumar. 2021. Water contamination by heavy metals and their toxic effect on aquaculture and human health through food chain. Letters in Applied NanoBioScience 10:2148–66. doi:10.33263/LIANBS102.21482166.
   Google Scholar
• Sprague, J. B. 1971. Measurement of pollutant toxicity to fish III. Sublethal effects and “safe” concentrations. Water Research 5:245–66. doi:10.1016/0043-1354(71.
   Web of Science ®Google Scholar
• Straus, D. L. 2003. The acute toxicity of copper to blue tilapia in dilutions of settled pond water. Aquaculture 219 (1–4):233–40. doi:10.1016/S0044-8486(02)00350-2.
   Web of Science ®Google Scholar
• Tao, S., A. Long, C. Liu, and R. Dawson. 2000. The influence of mucus on copper speciation in the gill microenvironment of carp (Cyprinus carpio). Ecotoxicology and Environmental Safety 47 (1):59–64. doi:10.1006/eesa.2000.1932.
   PubMed Web of Science ®Google Scholar
• Tavares-dias, M. 2021. Toxic, physiological, histomorphological, growth performance and antiparasitic effects of copper sulphate in fish aquaculture. Aquaculture 535:736350. doi:10.1016/j.aquaculture.2021.736350.
   Web of Science ®Google Scholar
• Taweel, A., M. Shuhaimi-Othman, and A. K. Ahmad. 2013. Assessment of heavy metals in tilapia fish (Oreochromis niloticus) from the langat river and engineering lake in Bangi, Malaysia, and evaluation of the health risk from tilapia consumption. Ecotoxicology and Environmental Safety 93:45–51. doi:10.1046/j.1439-0426.2003.00440.x.
   PubMed Web of Science ®Google Scholar
• Tunçsoy, M., S. Duran, Ö. Ay, B. Cicik, and C. Erdem. 2017. Effects of copper oxide nanoparticles on antioxidant enzyme activities and on tissue accumulation of Oreochromis niloticus. Bulletin of Environmental Contamination and Toxicology 99 (3):360–64. doi:10.1007/s00128-017-2129-z.
   PubMed Web of Science ®Google Scholar
• Ullah, A., H. Ur Rehman, S. Awais, M. Ahsan Sardar, A. Maalik, N. Muhammad, S. Zareen, M. Ateeq, W. Ahmad, F. Khan, et al. 2016. Investigation of acute toxicity and LC50 value of Cu for a fish Oreochromis niloticus. Journal of Entomology and Zoology Studies 4: 605–607.
   Google Scholar
• USEPA. 2016. Ecological effects test guidelines. OCSPP 850.1075 Fish acute toxicity test, freshwater and marine . United States Environmental Protection Agency. https://19january2017snapshot.epa.gov/sites/production/files/2015-07/documents/850-1075.pdf.
   Google Scholar
• Varanka, Z., I. Rojik, I. Varanka, J. Nemcsók, and M. Ábrahám. 2001. Biochemical and morphological changes in carp (Cyprinus carpio L.). Comparative Biochemistry and Physiology, Part C 128:467–78. doi:10.1016/s1532-0456(01)00166-1.
   PubMed Web of Science ®Google Scholar
• Walker, A. M., C. E. Copatti, F. V. S. T. Melo, and J. F. B. Melo. 2020. Metabolic and physiological responses to intraperitoneal injection of chromium oxide in hyperglycaemic Nile tilapia juveniles. Aquaculture 517:734821. doi:10.1016/j.aquaculture.2019.734821.
   Web of Science ®Google Scholar
• Wang, T., X. Long, Y. Cheng, Z. Liu, and S. Yan. 2015. A comparison effect of copper nanoparticles versus copper sulphate on juvenile Epinephelus coioides: Growth parameters, digestive enzymes, body composition, and histology as biomarkers. International Journal of Genomics 2015:783021. doi:10.1155/2015/783021.
   PubMed Web of Science ®Google Scholar
• Witeska, M. 2013. Erythrocytes in teleost fishes: A review. Zoology and Ecology 23 (4):275–81. doi:10.1080/21658005.2013.846963.
   Google Scholar
• Wolf, J. C., W. A. Baumgartner, V. S. Blazer, A. C. Camus, J. A. Engelhardt, J. W. Fournie, S. Frasca, D. B. Groman, M. L. Kent, L. H. Khoo, et al. 2015. Nonlesions, misdiagnoses, missed diagnoses, and other interpretive challenges in fish histopathology studies: A guide for investigators, authors, reviewers, and readers. Toxicologic Pathology 43 (3):297–325. doi:10.1590/S1676-06032009000400023.
   PubMed Web of Science ®Google Scholar