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Oxidative Stress in a Wild Population of the Freshwater Fish Hyphessobrycon Luetkenii Chronically Exposed to a Copper Mining Area: New Insights into Copper Toxicology

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Abstract

In this study, we examine markers of oxidative stress in the tetra Hyphessobrycon luetkenii collected from two locations in the copper contaminated João Dias creek (southern Brazil). Also, specimens were translocated from a clean reference section of the creek to a polluted stretch and vice-versa. Fish were held at in submerged cages for 96 h and then sacrificed. Nuclear abnormalities in erythrocytes and total antioxidant capacity, lipid peroxidation and protein carbonylation in gills, brain, liver and muscle displayed similar trends in both groups. Lipid peroxidation increased in all tissues of individuals translocated to the polluted site but only in liver and muscle of those translocated to the reference site. Increased protein carbonylation was also observed in gills of individuals translocated to the reference location. These results suggest similar oxidative stress among fish from the reference and polluted locations and that long-term metals exposure may require adaptations toward oxidative stress responses.

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References

  • Abril SIM, Altmüller J, Bianchini A, Nolte AW (2022) De novo transcriptome of the freshwater fish Hyphessobrycon luetkenii: Differential Gene expression in aggregates inhabiting an environment historically impacted by copper mining. Environ Toxicol Chem under review

  • Abril SIM, Costa PG, Bianchini A (2018a) Metal accumulation and expression of genes encoding for metallothionein and copper transporters in a chronically exposed wild population of the fish Hyphessobrycon luetkenii. Comp Biochem Physiol Part C 211:25–31. https://doi.org/10.1016/j.cbpc.2018.05.008

    Article  CAS  Google Scholar 

  • Abril SIM, Dalmolin C, Costa PG, Bianchini A (2018b) Expression of genes related to metal metabolism in the freshwater fish Hyphessobrycon luetkenii living in a historically contaminated area associated with copper mining. Environ Toxicol Pharmacol 60:146–156. https://doi.org/10.1016/j.etap.2018.04.019

    Article  CAS  Google Scholar 

  • ASTM (2014) Standard Guide for Conducting Acute Toxicity Tests on Test Materials with Fishes, Macroinvertebrates, and Amphibians. American Society for Testing and Materials. ASTM E729-96(2014), West Conshohocken, PA, USA

  • Barsiene J, Dedonyte V, Rybakovas A, Andreikenaite L, Andersen OK (2006) Investigation of micronuclei and other nuclear abnormalities in peripheral blood and kidney of marine fish treated with crude oil. Aquat Toxicol 78:99–104. https://doi.org/10.1016/j.aquatox.2006.02.022

    Article  CAS  Google Scholar 

  • Borges VD, Zebral YD, Costa PG, Fonseca JS, Klein RD, Bianchini A (2022) Metal accumulation and ion regulation in the fish Hyphessobrycon luetkenii living in a site chronically contaminated by copper: insights from translocation experiments. Arch Environ Contam Toxicol 82:62–71. https://doi.org/10.1007/s00244-021-00895-3

    Article  CAS  Google Scholar 

  • Buchheister A, Latour RJ (2010) Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can J Fish Aquat Sci 67:445–461. https://doi.org/10.1139/F09-196

    Article  CAS  Google Scholar 

  • Busst GMA, Britton JR (2018) Tissue-specific turnover rates of the nitrogen stable isotope as functions of time and growth in a cyprinid fish. Hydrobiologia 805:49–60. https://doi.org/10.1007/s10750-017-3276-2

    Article  CAS  Google Scholar 

  • Chakraborty SB, Mazumdar D, Banerjee S (2010) Determination of ideal stocking density for cage culture of monosex Nile tilapia (Oreochromis niloticus) in India. Proc Zool Soc 63:53–59. https://doi.org/10.1007/s12595-010-0007-3

    Article  Google Scholar 

  • CONAMA (2005) Conselho Nacional do Meio Ambiente, Resolução nº 357, Brasília, DF, Brazil. http://conama.mma.gov.br/?option=com_sisconama&task=arquivo.download&id=450

  • Fauconneau B, Arnal M (1985) In vivo protein synthesis in different tissues and the whole body of rainbow trout (Salmo gairdnerii R.). Influence of environmental temperature. Comp Biochem Physiol A Comp Physiol 82:179–187. https://doi.org/10.1016/0300-9629(85)90723-6

    Article  CAS  Google Scholar 

  • Grosell M (2011) Copper. In: Wood CM, Farrell T, Brauner CJ (eds) Homeostasis and toxicology of essential Metals, Fish Physiology, vol 31A. Academic Press, San Diego, pp 53–133. https://doi.org/10.1016/S1546-5098(11)31002-3

    Chapter  Google Scholar 

  • Gusso-Choueri PK, Choueri RB, Araújo GS, Cruz ACF, Stremel T, Campos S, Abessa DMS, Ribeiro CAO (2015) Assessing pollution in marine protected areas: the role of a multi-biomarker and multi-organ approach. Environ Sci Pollut Res 22:18047–18065. https://doi.org/10.1007/s11356-015-4911-y

    Article  CAS  Google Scholar 

  • Haverroth GM, Welang C, Mocelin RN, Postay D, Bertoncello KT, Franscescon F, Rosemberg DB, Dal Magro J, Dalla Corte CL (2015) Copper acutely impairs behavioral function and muscle acetylcholinesterase activity in zebrafish (Danio rerio). Ecotoxicol Environ Saf 122:440–447. https://doi.org/10.1016/j.ecoenv.2015.09.012

    Article  CAS  Google Scholar 

  • Houlihan DF, Mathers EM, Foster A (1993) Biochemical correlates of growth rate in fish. In: Rankin JC, Jensen FB (eds) Fish Ecophysiology. Chapman & Hall Fish and Fisheries Series, vol 9. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-2304-4_2

    Chapter  Google Scholar 

  • Kalay M, Canli M (2000) Elimination of essential (Cu, Zn) and non-essential (Cd, pb) metals from tissues of a freshwater fish Tilapia zilli. Turk J Zool 24:429–436

    CAS  Google Scholar 

  • Koh HL, The SY, Lee E, Tan WK, Sagathevan KA, Low AA (2018) Derivation of optimal fish stocking density via simulation of water quality model E2Algae. AIP Conference Proceedings 1974, 020042. https://doi.org/10.1063/1.5041573

  • Malhotra N, Ger TR, Uapipatanakul B, Huang JC, Chen KH, Hsiao CD (2020) Review of copper and copper nanoparticle toxicity in fish. Nanomaterials 10:1126. https://doi.org/10.3390/nano10061126

    Article  CAS  Google Scholar 

  • Matley JK, Fisk AT, Tobin AJ, Heupel MR, Simpfendorfer CA (2016) Diet-tissue discrimination factors and turnover of carbon and nitrogen stable isotopes in tissues of an adult predatory coral reef fish, Plectropomus leopardus. Rapid Commun Mass Spectrom 30:29–44. https://doi.org/10.1002/rcm.7406

  • Møller IM, Rogowska-Wrzesinska A, Rao RS (2011) Protein carbonylation and metal-catalyzed protein oxidation in a cellular perspective. J Proteom 74:2228–2242. https://doi.org/10.1016/j.jprot.2011.05.004

    Article  CAS  Google Scholar 

  • Monk CT, Chéret B, Czapla P, Hühn D, Klefoth T, Eschbach E, Hagemann R, Arlinghaus R (2020) Behavioural and fitness effects of translocation to a novel environment: whole-lake experiments in two aquatic top predators. J Anim Ecol 89:2325–2344. https://doi.org/10.1111/1365-2656.13298

    Article  Google Scholar 

  • Oakes KD, Van De Kraak GJ (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–463. https://doi.org/10.1016/s0166-445x(02)00204-7

    Article  CAS  Google Scholar 

  • Radi AA, Hai DQ, Matkovics B (1986) Comparative antioxidant enzyme study in freshwater fishes. II. Distribution of antioxidant enzymes and lipid peroxidation in omnivorous fish organs. Acta Biol Hung 37:135–141

    CAS  Google Scholar 

  • Radi AA, Hay DQ, Gabrielak T, Matkovics B (1985) Comparative antioxidant enzyme study in freshwater fishes. I. distribution of superoxide dismutase, peroxide-decomposing enzymes and lipid peroxidation in herbivorous fishes. Acta Biol Hung 36:169–174

    CAS  Google Scholar 

  • Sanz A, Trenzado CE, Botello Castro H, López-Rodríguez MJ, Tierno de Figueroa JM (2013) Relationship between brain and liver oxidative state and maximum lifespan potential of different fish species. Comp Biochem Physiol A Mol Integr Physiol 165:358–364. https://doi.org/10.1016/j.cbpa.2013.04.019

    Article  CAS  Google Scholar 

  • Simonato JD, Mela M, Doria HB, Guiloski IC, Randi MAF, Carvalho PSM, Meletti PC, Silva de Assis HC, Bianchini A, Martinez CBR (2016) Biomarkers of waterborne copper exposure in the neotropical fish Prochilodus lineatus. Aquat Toxicol 170:31–41

    Article  CAS  Google Scholar 

  • Smith RW, Houlihan DF (1995) Protein synthesis and oxygen consumption in fish cells. J Comp Physiol B 165:93–101. https://doi.org/10.1007/BF00301473

    Article  CAS  Google Scholar 

  • Sung J, Lee J, Lee S (2020) Exposure to copper (II) chloride induces behavioral and endocrine changes in zebrafish. J Life Sci 30:321–330. https://doi.org/10.5352/JLS.2020.30.4.321

    Article  Google Scholar 

  • Tavares-Dias M (2021) Toxic, physiological, histomorphological, growth performance and antiparasitic effects of copper sulphate in fish aquaculture. Aquaculture 535:736350. https://doi.org/10.1016/j.aquaculture.2021.736350

    Article  CAS  Google Scholar 

  • Xia B, Gao QF, Dong SL, Wang F (2013) Turnover and fractionation of nitrogen stable isotope in tissues of grass carp Ctenopharyngodon idellus. Aquac Environ Interact 3:177–186. https://doi.org/10.3354/aei00061

    Article  Google Scholar 

  • Zebral YD, Anni ISA, Afonso SB, Abril SIM, Klein RD, Bianchini A (2018) Effects of life-time exposure to waterborne copper on the somatotropic axis of the viviparous fish Poecilia vivipara. Chemosphere 203:410–417. https://doi.org/10.1016/j.chemosphere.2018.03.202

    Article  CAS  Google Scholar 

  • Zebral YD, Roza M, Fonseca JS, Costa PG, Oliveira CS, Zocke TG, Dal Pizzol JL, Robaldo RB, Bianchini A (2019) Waterborne copper is more toxic to the killifish Poecilia vivipara in elevated temperatures: linking oxidative stress in the liver with reduced organismal thermal performance. Aquat Toxicol 209:142–149. https://doi.org/10.1016/j.aquatox.2019.02.005

    Article  CAS  Google Scholar 

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Acknowledgements

Thanks to Dr. Sandra I. M. Abril for her help in the field experiment. The present study was supported by grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Instituto Nacional de Ciência e Tecnologia de Toxicologia Aquática, Brasília, DF, Brazil. grant #573949/2008-5) and the International Development Research Centre (IDRC, Ottawa, ON, Canada, grant #104519-027). A. Bianchini (Proc. # 311410/2021-9) is a research fellow from the Brazilian CNPq and was supported by the International Canada Research Chair Program (IDRC).

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Borges, V.D., Zebral, Y.D., Costa, P.G. et al. Oxidative Stress in a Wild Population of the Freshwater Fish Hyphessobrycon Luetkenii Chronically Exposed to a Copper Mining Area: New Insights into Copper Toxicology. Bull Environ Contam Toxicol 110, 77 (2023). https://doi.org/10.1007/s00128-023-03721-9

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