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Multibiomarker toxicity characterization of uranium mine drainages to the fish Carassius auratus

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Abstract

The release of acidic effluents, naturally enriched in metals and radionuclides, is the main legacy of uranium mines. Generally, metals dissolved by these acidic effluents can cause significant alterations in exposed organisms, with distinct toxicological outcomes. In this study, 72 individuals of the freshwater fish species Carassius auratus were exposed in situ for different periods (8, 16, 24, and 48 h) to water from a pond (treatment pond (TP)) with a chemically treated effluent and a reference pond (PRP), in the vicinity of the Cunha Baixa uranium mine (Portugal). Comparing the water of the two ponds, the PRP pond was characterized by higher pH and oxygen values and lower conductivity and hardness values. Regarding total metal concentrations, among others, magnesium (56,000 μg/L), sodium (17,400 μg/L), zinc (86 μg/L), manganese (6340 μg/L), and uranium (1380 μg/L) concentrations in the TP pond were above the values obtained for the PRP pond. The values of manganese and uranium exceeded the values of quality criteria established for surface waters for cyprinids and for irrigation purposes. After exposure to pond water, significant differences were recorded for several biomarkers: (i) between ponds for acetylcholinesterase (AChE) with higher activities for animals from the PRP and glutathione-S-transferase (GST) activities that were particularly enhanced in animals from the TP pond; (ii) between ponds and exposure periods for lactate dehydrogenase (LDH) activity, since organisms from PRP pond presented always higher values than those from the TP pond, and among these, organisms exposed for the longer period presented a further depression in LDH activity; and (iii) between exposure periods for erythrocyte micronucleus. GSTs and LDH were the most sensitive biomarkers within the timeframe of the in situ assay performed. Despite the alleged efficacy of the chemical treatment (evidenced by a significantly lower pH), some metals persisted in the treated effluent (TP pond), potentially contributing to the induction of oxidative stress or increased conjugation metabolic activity in fish.

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References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 6:105–121

    Google Scholar 

  • Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1519:37–48

    Article  Google Scholar 

  • Antunes SC, Pereira R, Gonçalves F (2007) Acute and chronic toxicity of effluent water from an abandoned uranium mine. Arch Environ Contam Toxicol 53:207–213

    Article  CAS  Google Scholar 

  • Antunes SC, Castro BB, Pereira R, Gonçalves F (2008) Contribution for tier I of the ecological risk assessment of Cunha Baixa uranium mine (Central Portugal): II soil ecotoxicological screening. Sci Total Environ 390:387–395

    Article  CAS  Google Scholar 

  • APHA (1995) Standard methods for the examination of water and wastewater, 19th edn

    Google Scholar 

  • ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E-790-80 Annual Book of ASTM Standards. American Society for Testing and Materials, Philadelphia

    Google Scholar 

  • Barata C, Lekumberri I, Vila-Escalé M, Prat N, Porte C (2005) Trace metal concentration, antioxidant enzyme activities and susceptibility to oxidative stress in the tricoptera larvae Hydropsyche exocellata from the Llobregat river basin (NE Spain). Aquat Toxicol 74:3–19

    Article  CAS  Google Scholar 

  • Baršienè J, Dedonytė V, Rybakovas A, Andreikėnaitė 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 78S:99–104

    Article  Google Scholar 

  • Bolognesi C, Perrone E, Roggieri P, Pampanin D, Sciutto A (2006) Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquat Toxicol 78S:93–98

    Article  Google Scholar 

  • Brandão F, Correia AT, Gonçalves F, Nunes B (2013) Effects of anthropogenic metallic contamination on cholinesterases of Gambusia holbrooki. Mar Pollut Bull 76(1–2):72–76

    Article  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bussy C, Lestaevel P, Dhieux B, Amourette C, Paquet F, Gourmelon P, Houpert P (2006) Chronic ingestion of uranyl nitrate perturbs acetylcholinesterase activity and monoamine metabolism in male rat brain. Neurotoxicology 27:245–252

  • Canli EG, Canli M (2015) Low water conductivity increases the effects of copper on the serum parameters in fish (Oreochromis niloticus). Envir Toxicol Pharmacol 39:606–613

    Article  CAS  Google Scholar 

  • Carrasco KR, Tilbury KL, Myers MS (1990) Assessment of the piscine micronuclei test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci 47:2123–2136

    Article  CAS  Google Scholar 

  • Carvalho FP, Madruga MJ, Reis MC, Alves JG, Oliveira JM, Gouveia J, Silva L (2007) Radioactivity in the environment around past radium and uranium mining sites of Portugal. J Environ Radioact 96:39–46

    Article  CAS  Google Scholar 

  • Carvalho CS, Bernusso VA, Fernandes MN (2015) Copper levels and changes in pH induce oxidative stress in the tissue of curimbata (Prochilodus lineatus). Aquat Toxicol 167:220–227

    Article  CAS  Google Scholar 

  • Castro BB, Sobral O, Guilhermino L, Ribeiro R (2004) An in situ bioassay integrating individual and biochemical responses using small fish species. Ecotoxicology 13:667–681

    Article  CAS  Google Scholar 

  • Çavaş T, Ergene-Gözükara S (2003) Micronuclei, nuclear lesions and interphase silver-stained nucleolar organizer regions (AgNORs) as cyto-genotoxicity indicators in Oreochromis niloticus exposed to textile mill effluent. Mutat Res 538:81–91

    Article  Google Scholar 

  • Çavaş T, Ergene-Gözükara S (2005) Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat Toxicol 74:264–271

    Article  Google Scholar 

  • Charron L, Geffard O, Chaumot A, Coulaud R, Queau H, Geffard A, Dedourge-Geffard O (2013) Effect of water quality and confounding factors on digestive enzyme activities in Gammarus fossarum. Environ Sci Pollut Res Int 20(12):9044–56

    Article  CAS  Google Scholar 

  • Coulaud R, Geffard O, Xuereb B, Lacaze E, Quéau H, Garric J, Charles S, Chaumot A (2011) In situ feeding assay with Gammarus fossarum (Crustacea): modelling the influence of confounding factors to improve water quality biomonitoring. Water Res 45(19):6417–6429

    Article  CAS  Google Scholar 

  • de la Torre FR, Salibián A, Ferrari L (2007) Assessment of the pollution impact on biomarkers of effect of a freshwater fish. Chemosphere 68:582–1590

    Google Scholar 

  • Dautremepuits C, Betoulle S, Vernet G (2002) Antioxidant response modulated by copper in healthy or parasitized carp (Cyprinus carpio L.) by Ptychobothrium sp. (Cestoda). Biochim Biophys Acta 1573:4–8

    Article  CAS  Google Scholar 

  • Dogan Z, Eroglu A, Kanak EG, Atli G, Canli M (2014) Response of antioxidant system of tilapia (Oreochromis niloticus) following exposure to chromium and copper in differing hardness. Bull Environ Contam Toxicol 92:680–686

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Elumalai M, Antunes C, Guilhermino L (2002) Effects of single metals and their mixtures on selected enzymes of Carcinus maenas. Water Air Soil Poll 141:273–280

    Article  CAS  Google Scholar 

  • Elumalai M, Antunes C, Guilhermino L (2007) Enzymatic biomarkers in the crab Carcinus maenas from the Minho River estuary (NW Portugal) exposed to zinc and mercury. Chemosphere 66:1249–1255

    Article  CAS  Google Scholar 

  • Frasco MF, Guilhermino L (2002) Effects of dimethoate and beta-naphthoflavone on selected biomarkers of Poecilia reticulata. Fish Physiol Biochem 26:149–156

    Article  CAS  Google Scholar 

  • Freitas DRJ, Rosa RM, Moraes J, Campos E, Logullo C, Da Silva Vaz Jr I, Masuda A (2007) Relationship between glutathione-S-transferase, catalase, oxygen, consumption, lipid peroxidation and oxidative stress in eggs and larvae of Boophilus microplus (Acarina: Ixodidae). Comp Biochem Physiol A 146:688–694

    Article  CAS  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45

    Article  CAS  Google Scholar 

  • Guilherme S, Válega M, Pereira ME, Santos MA, Pacheco M (2008) Erythrocytic nuclear abnormalities in wild and caged fish (Liza aurata) along an environmental mercury contamination gradient. Ecotoxicol Environ Saf 70:411–421

    Article  CAS  Google Scholar 

  • Gustavino B, Scornajenghi KA, Minissi S, Ciccotti E (2001) Micronuclei induced in erythrocytes of Cyprinus carpio (teleostei, pisces) by X-rays and colchicines. Mutat Res 494:151–159

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione-S-transferases—the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Hodgson E, Levi P (2004) Hepatotoxicity. In: Hodgson E (ed) A textbook of modern toxicology. Wiley Interscience, New Jersey, pp 263–272

    Chapter  Google Scholar 

  • INAG (2009) Critérios para a Classificação do Estado de Massas de Água Superficiais – Rios e Albufeiras. Instituto da Água, IP. Ministério do Ambiente, do Ordenamento do Território e do Desenvolvimento Regional. Lisboa, Portugal

  • Lange B, Vejdelek ZJ (1980) Photometrische Analyse. Verlag Chemie, Weinheim

    Google Scholar 

  • Leblanc GA (2004) Acute toxicity. In: Hodgson E (ed) A textbook of modern toxicology. Wiley Interscience, New Jersey, pp 215–224

    Google Scholar 

  • Lemos CT, Rödel PM, Terra NR, Oliveira NCA, Erdtmann B (2007) River water genotoxicity evaluation using micronucleus assay in fish erythrocytes. Ecotoxicol Environ Saf 66:391–401

    Article  Google Scholar 

  • Liu H, Wang W, Zhang J, Wang X (2006) Effects of copper and its ethylenediaminetetraacetate complex on the antioxidant defenses of the goldfish, Carassius auratus. Ecotoxicol Environ Saf 65:350–354

    Article  CAS  Google Scholar 

  • Lourenço J, Pereira R, Silva A, Morgado J, Carvalho F, Oliveira J, Malta M, Paiva A, Mendo S, Gonçalves F (2011) Genotoxic endpoints in the earthworms sub-lethal assay to evaluate natural soils contaminated by metals and radionuclides. J Hazard Mater 186:788–795

    Article  Google Scholar 

  • Lourenço J, Pereira R, Silva A, Carvalho F, Oliveira J, Malta M, Paiva A, Gonçalves F, Mendo S (2012) Evaluation of the sensitivity of genotoxicity and cytotoxicity endpoints in earthworms exposed in situ to uranium mining wastes. Ecotoxicol Environ Saf 75:46–54

    Article  Google Scholar 

  • Lushchak OV, Kubrak OI, Lozinsky OV, Storey JM, Storey KB, Lushchak VI (2009) Chromium (III) induces oxidative stress in goldfish liver and kidney. Aquat Toxicol 93:45–52

    Article  CAS  Google Scholar 

  • MA (1998) Decreto lei n° 236/98 de 1 de Agosto. Ministério do Ambiente. Diário da República I série, A 176:3676-3722

  • MAOT (2010) Decreto-Lei n.º 103/2010 de 24 de Setembro. Ministério do Ambiente e do Ordenamento do Território. Diário da República I série 187:4289–4296. Lisboa, Portugal

  • Marques SM, Antunes SC, Pissarra H, Pereira ML, Gonçalves F, Pereira R (2009) Histopathological changes and erytrocytic nuclear abnormalities in Iberian green frogs (Rana perezi Seoane) from a uranium mine pond. Aquat Toxicol 91:187–195

    Article  CAS  Google Scholar 

  • Marques SM, Antunes SC, Nunes B, Gonçalves F, Pereira R (2011) Antioxidant response and metal accumulation in tissues of Iberian green frogs (Pelophylax perezi) inhabiting a deactivated uranium mine. Ecotoxicology 20:1315–1327

    Article  CAS  Google Scholar 

  • Michaelidis B, Spring A, Pörtner HO (2007) Effects of long-term acclimation to environmental hypercapnia on extracellular acid–base status and metabolic capacity in Mediterranean fish Sparus aurata. Mar Biol 150:1417–1429

    Article  Google Scholar 

  • Minissi S, Ciccotti E, Rizzoni M (1996) Micronucleus test in erythrocytes of Barbus plebejus (Teleostei, Pisces) from two natural environments: a bioassay for the in situ detection of mutagens in freshwater. Mutat Res 367:245–251

    Article  CAS  Google Scholar 

  • Nunes B, Caldeira C, Pereira J, Gonçalves F, Correia AT (2015a). Chronic effects of realistic concentrations of non-essential and essential metals (lead and zinc) on oxidative stress biomarkers of the mosquitofish, Gambusia holbrooki. Archives of Environmental Contamination and Toxicology 69(4):586-95. doi: 10.1007/s00244-015-0190-3.

  • Nunes B, Caldeira C, Pereira JL, Gonçalves F, Correia AT (2015b). Perturbations in ROS-related processes of the fish Gambusia holbrooki after acute and chronic exposures to the metals copper and cadmium. Environmental Science and Pollution Research 22(5):3756-65.

  • Nunes B, Capela RC, Rodrigues S, Caldeira C, Gonçalves F, Correia AT (2014a). Chronic effects of lead, copper, zinc, and cadmium on biomarkers of the European eel, Anguilla anguilla. Environmental Science and Pollution Research 21(8):5689-700.

  • Nunes B, Barbosa AR, Antunes SC, Gonçalves F (2014b) Combination effects of anticholinesterasics in acetylcholinesterase of a fish species: effects of a metallic compound, an organophosphate pesticide and a pharmaceutical drug. Environmental Science and Pollution Research 21(9):6258-62.

  • Nunes B (2011) The use of cholinesterases in ecotoxicology. Rev Environ Contam Toxicol 212:29–59

    CAS  Google Scholar 

  • Nunes B, Carvalho F, Guilhermino L (2006) Effects of widely used pharmaceuticals and a detergent on a oxidative stress biomarkers of the crustacean Artemia parthenogenetica. Chemosphere 62:581–594

    Article  CAS  Google Scholar 

  • Oliva M, Perales JA, Gravato C, Guilhermino L, Galindo-Riaño MD (2012) Biomarkers responses in muscle of Senegal sole (Solea senegalensis) from a heavy metals and PAHs polluted estuary. Mar Pollut Bull 64(10):2097–2108

    Article  CAS  Google Scholar 

  • Oliveira JMS, Ávila PF (2001) Geochemistry of the surrounding area of Cunha Baixa uranium mine (Mangualde, Centre of Portugal). Estudos, Notas e Trabalhos, Tomo 43. Instituto Geológico e Mineiro. Lisboa, Portugal

  • Ozmen M, Güngördü A, Kucukbay Z, Güler RE (2006) Monitoring the effects of water pollution on Cyprinus carpio in Karakaya Dam Lake, Turkey. Ecotoxicology 15:157–169

    Article  CAS  Google Scholar 

  • Pereira AMM, Soares AMVM, Gonçalves F, Ribeiro R (2000) Water-column, sediment, and in situ chronic bioassays with cladocerans. Ecotoxicol Environ Saf 47:27–38

    Article  CAS  Google Scholar 

  • Pereira R, Antunes SC, Marques SM, Gonçalves F (2008) Contribution for tier I of the ecological risk assessment of Cunha Baixa uranium mine (Central Portugal): I soil chemical characterization. Sci Total Environ 390:377–386

    Article  CAS  Google Scholar 

  • Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge, p 537

    Book  Google Scholar 

  • Rao JV (2006) Biochemical alterations in euryhaline fish, Oreochromis mossambicus exposed to sub-lethal concentrations of an organophosphorus insecticide, monocrotophos. Chemosphere 65:814–1820

    Google Scholar 

  • Richetti SK, Rosemberg DB, Ventura-Lima J, Monserrat JM, Bogo MR, Bonan CD (2011) Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. Neurotoxicology 32:116–122

  • Saglam D, Atli G, Canli M (2013) Investigations on the osmoregulation of freshwater fish (Oreochromis niloticus) following exposures to metals (Cd, Cu) in differing hardness. Ecotoxicol Environ Saf 92:79–86

    Article  CAS  Google Scholar 

  • Sanchez W, Palluel O, Meunier L, Coquery M, Porcher J, Aït-Aïssa S (2005) Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ Toxicol Pharmacol 19:177–183

    Article  CAS  Google Scholar 

  • Santos D, Milatovic D, Andrade V, Batoreu MC, Aschner M, Marreilha dos Santos AP (2012) The inhibitory effect of manganese on acetylcholinesterase activity enhances oxidative stress and neuroinflammation in the rat brain. Toxicology 292:90–98

    Article  CAS  Google Scholar 

  • Santos Oliveira JM, Ávila PF (1998) Geochemistry study in the surrounding area of Cunha Baixa mine (Mangualde, Centre of Portugal). Relatório do Instituto Geológico e Mineiro. Lisboa, Portugal

  • Schrader M, Fahimi HD (2006) Peroxisomes and oxidative stress. Biochim Biophys Acta 1763:1755–1766

    Article  CAS  Google Scholar 

  • Sen A, Semiz A (2007) Effects of metals and detergents on biotransformation and detoxification enzymes of leaping mullet (Liza saliens). Ecotoxicol Environ Saf 68:405–411

    Article  CAS  Google Scholar 

  • Sheppard SC, Sheppard MI, Gallerand M-O, Sanipelli B (2005) Derivation of ecotoxicity thresholds for uranium. J Environ Radioact 79:55–83

    Article  Google Scholar 

  • Stegeman JJ, Brouwer M, Di Giulio RT, Förlin L, Fowler BA, Sanders BM, Van Veld PA (1992) Molecular responses to environmental contamination: enzyme and protein systems as indicators of chemical exposure and effect. In: Huggett RJ, Kimerle RA, Mehrle PM Jr, Bergman HL (eds) Biomarkers. Biochemical, physiological, and histological markers of anthropogenic stress. The SETAC Publication Series Lewis Publishers, Chelsea, pp 235–336

    Google Scholar 

  • Stoiber T, Bonacker D, Böhm K, Bolt H, Thier R, Degen G, Unger E (2004) Disturbed microtubule function and induction of micronuclei by chelate complexes of mercury (II). Mutat Res 563:97–106

    Article  CAS  Google Scholar 

  • Sun Y, Yu H, Zhang J, Yin Y, Shen H, Lui H, Wang X (2006) Bioaccumulation and antioxidant responses in goldfish Carassius auratus under HC Orange No. 1 exposure. Ecotoxicol Environ Saf 63:430–437

    Article  CAS  Google Scholar 

  • Tilton FA, Bammler TK, Gallagher EP (2011) Swimming impairment and acetylcholinesterase inhibition in zebrafish exposed to copper or chlorpyrifos separately, or as mixtures. Comp Biochem Physiol Part C: Toxicol Pharmacol 153(1):9–16

    Google Scholar 

  • Udroiu I (2006) The micronucleus test in piscine erythrocytes. Aquat Toxicol 79:201–204

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Vassault A (1983) Lactate dehydrogenase. Method Enzym Anal 3:118–126

    CAS  Google Scholar 

  • Wu RSS, Lam PKS (1997) Glucose-6-phosphate dehydrogenase and lactate dehydrogenase in the green-lipped mussel (Perna viridis): possible biomarkers for hypoxia in the marine environment. Wat Res 31:2797–2801

    Article  CAS  Google Scholar 

  • Yi MQ, Liu HX, Shi XY, Liang P, Gao XW (2006) Inhibitory effects of four carbamate insecticides on acetylcholinesterase of male and female Carassius auratus in vitro. Comp Biochem Physiol C 143:113–116

    Article  CAS  Google Scholar 

  • Yi X, Ding H, Lu Y, Liu H, Zhang M, Jiang W (2007) Effects of long-term alachlor exposure on hepatic antioxidant defense and detoxifying enzyme activities in crucian carp (Carassius auratus). Chemosphere 68:1576–1581

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partially funded by Fundação para a Ciência e a Tecnologia—POCI 2010 and FEDER (POCI/AMB/60899/2004 and PPCDT/AMB/60899/2004). Thanks are due for the financial support to CESAM (UID/AMB/50017), to FCT/MEC through national funds, and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020.

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  1. Departamento de Biologia, Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    M. L. Bessa, F. J. M. Gonçalves & B. Nunes

  2. Centro de Estudos do Ambiente e do Mar (CESAM), Universidade de Aveiro, Campus Universitário de Santiago, 3810-193, Aveiro, Portugal

    M. L. Bessa, F. J. M. Gonçalves & B. Nunes

  3. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre s/no., 4169-007, Porto, Portugal

    S. C. Antunes & R. Pereira

  4. Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Universidade do Porto, Rua dos Bragas 289, 4050-123, Porto, Portugal

    S. C. Antunes & R. Pereira

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  1. M. L. Bessa
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Bessa, M.L., Antunes, S.C., Pereira, R. et al. Multibiomarker toxicity characterization of uranium mine drainages to the fish Carassius auratus . Environ Sci Pollut Res 23, 13355–13367 (2016). https://doi.org/10.1007/s11356-016-6426-6

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