Skip to main content

Advertisement

Log in

Iron and manganese present in underground water promote biochemical, genotoxic, and behavioral alterations in zebrafish (Danio rerio)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Iron (Fe) and manganese (Mn) are metals commonly found at high concentrations in underground water. These metals are essential for the good functioning of living organisms, but high concentrations lead to imbalance, potentiating the appearance of pathologies. This study aimed to evaluate the effect of exposure to naturally occurring metals in groundwater, using zebrafish (Danio rerio) as an experimental model. Thus, zebrafish were exposed to Fe (0.8 and 1.3 mg/L), Mn (0.2 and 0.4 mg/L), and groundwater collected from deep tube wells with Fe and Mn (Fe 0.8/Mn 0.2 mg/L and Fe 1.3/Mn 0.4 mg/L) for 30 days. Bioaccumulation of these metals has been demonstrated in the livers and muscles of zebrafish. Acetylcholinesterase activity changed only in zebrafish muscles in all groups. Sulfhydryl levels changed mainly in the group Mn 0.4. SOD/CAT ratio decreased in the groups Fe 0.8 and 1.3, Mn 0.4, and Fe 0.8/Mn 0.4. An increase in the frequency of micronucleus in all groups was shown as a consequence of these changes. Behavioral parameters (time and distance traveled, mean speed, turn angle, latency, and number of crossings between compartments) have also changed, mainly in the groups Fe 1.3, Mn 0.4, and Fe 1.3/Mn 0.4. Therefore, long-term exposure to Fe and Mn, even at not so high concentrations, may cause biochemical, genotoxic, and behavioral changes in zebrafish.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymology 105:21–126

    Google Scholar 

  • Ahmad I (2001) Catalase. In: Buettner, G.R., Oberley, L.W. (Orgs.). Free radicals in biology and medicine program. University of Iowa: Iowa

  • Al-Sabti K, Metcalfe CD (1995) Fish micronuclei for assessing genotoxicity in water. Genet Toxicol 343:121–135

    Article  CAS  Google Scholar 

  • Altenhofen S, Wiprich MT, Nery LR, Leite CE, Vianna MRMR, Bonan CD (2017) Manganese(II) chloride alters behavioral and neurochemical parameters in larvae and adult zebrafish. Aquat Toxicol 182:172–183. https://doi.org/10.1016/j.aquatox.2016.11.013

    Article  CAS  Google Scholar 

  • Anbumani S, Mohankumar MN (2012) Gamma radiation induced micronuclei and erythrocyte cellular abnormalities in the fish Catla catla. Aquat Toxicol 122-123:125–132. https://doi.org/10.1016/j.aquatox.2012.06.001

    Article  CAS  Google Scholar 

  • APHA/AWWA/WEF (American Public Health Association/American Water Works Association/Water Environment Federation) (2011) 1060 Collection and Preservation of Samples

  • Arias ARL, Buss DF, de AC, Inácio AF, Freire MM, Egler M, Mugnai R, Baptista DF (2007) Utilização de bioindicadores na avaliação de impacto e no monitoramento da contaminação de rios e córregos por agrotóxicos. Ciência & Saúde Coletiva 12(1):61–72

    Article  Google Scholar 

  • ATSDR (Agency for Toxic Substances and Disease Registry) (2012) Toxicological profile for manganese. Public comment. U.S. Public Health Service, U.S. Department of Health and Human Services, Atlanta

    Google Scholar 

  • Baird C, Cann M (2011) Química ambiental. Bookman, Porto Alegre

    Google Scholar 

  • Belaidi AA, Bush AI (2016) Iron neurochemistry in Alzheimer’s disease and Parkinson’s disease: targets for therapeutics. J Neurochem 139(1):179–197. https://doi.org/10.1111/jnc.13425

    Article  CAS  Google Scholar 

  • Benites LM, Doncato KB, Minho T dos S, Perazzo GX (2014) Avaliação do potencial mutagênico de cobre da água do rio Uruguai. Ciência e Natura 36(2):107–113. https://doi.org/10.5902/2179460X13610

    Article  Google Scholar 

  • Bicudo CE d M, Tundisi JG, Scheuenstuhl MCB (2010) Águas do Brasil: análises estratégicas. Instituto de Botânica, São Paulo

    Google Scholar 

  • Bittencourt AVL, Rosa Filho EF, Hindi EC, Buchmann Filho AC (2003) A influência dos basaltos e de misturas com águas de aquíferos sotopostos nas águas subterrâneas do sistema aquífero serra geral na bacia do rio piquiri, Paraná. BR Rev Águas Subterrâneas 1(17):67–76. https://doi.org/10.14295/ras.v17i1.1313

    Article  Google Scholar 

  • Blaser RE, Rosemberg D (2012) Measures of anxiety in zebrafish (Danio rerio): dissociation of black/white preference and novel tank test. PLoS One 7(5):e36931. https://doi.org/10.1371/journal.pone.0036931

    Article  CAS  Google Scholar 

  • Borghetti NRB, Borghetti JR, Rosa Filho EF (2011) A integração das águas: Revelando o verdadeiro aquífero guarani. Edição da Autora, Curitiba

    Google Scholar 

  • Bouabid S, Tinakoua A, Lakhdar-Ghazal N, Benazzouz A (2016) Manganese neurotoxicity: behavioral disorders associated with dysfunctions in the basal ganglia and neurochemical transmission. J Neurochem 136:677–691. https://doi.org/10.1111/jnc.13442

    Article  CAS  Google Scholar 

  • Bowman AB, Kwakye GF, Hernández EH, Aschner M (2011) Role of manganese in neurodegenerative diseases. J Trace Elem Med Biol 25(4):191–203. https://doi.org/10.1016/j.jtemb.2011.08.144

    Article  CAS  Google Scholar 

  • Bresciani G, da Cruz IBM, González-Gallego J (2015) Manganese superoxide dismutase and oxidative stress modulation. Adv Clin Chem 68:87–130. https://doi.org/10.1016/bs.acc.2014.11.001

    Article  CAS  Google Scholar 

  • Burtis CA, Ashwood ER, Bruns DE (2008) Tietz: Fundamentos de química clínica. Elsevier, Rio de Janeiro

    Google Scholar 

  • Carasek F (2016) Qualidade da água subterrânea do sistema aquífero serra geral na região oeste do estado de Santa Catarina, Brasil. Dissertation. Universidade Comunitária da Região de Chapecó, Chapecó

    Google Scholar 

  • Caudle WM (2017) Occupational metal exposure and parkinsonism. Adv Neurobiol 18:143–158. https://doi.org/10.1007/978-3-319-60189-2_7

    Article  Google Scholar 

  • CETESB (Companhia Ambiental do Estado de São Paulo) (2012) Água subterrânea e poços tubulares. CETESB, São Paulo

    Google Scholar 

  • Chtourou Y, Fetoui H, Sefi M, Trabelsi K, Barkallah M, Boudawara T, Kallel H, Zeghal N (2010) Silymarin, a natural antioxidant, protects cerebral cortex against manganese-induced neurotoxicity in adult rats. Biometals. 23(6):985–996. https://doi.org/10.1007/s10534-010-9345-x

    Article  CAS  Google Scholar 

  • Chua AC, Morgan EH (1996) Effects of iron deficiency and iron overload on manganese uptake and deposition in the brain and other organs of the rat. Biol Trace Elem Res 55(1–2):39–54

    Article  CAS  Google Scholar 

  • Copaja SV, Pérez CA, Vega-Retter C, Véliz D (2017) Heavy metal content in Chilean fish related to habitat use, tissue type and river of origin. Bull Environ Contam Toxicol 99(6):695–700. https://doi.org/10.1007/s00128-017-2200-9

    Article  CAS  Google Scholar 

  • Crossgrove J, Zheng W (2004) Manganese toxicity upon overexposure. NMR Biomed 17:544–553. https://doi.org/10.1002/nbm.931

    Article  CAS  Google Scholar 

  • Dal Santo GD, Grotto A, Boligon AA, Da Costa B, Rambo CL, Fantini EA, Sauer E, Lazzarotto LMV, Bertoncello KT, Júnior OT, Garcia SC, Siebel AM, Rosemberg DB, Magro JD, Conterato GMM, Zanatta L (2018) Protective effect of Uncaria tomentosa extract against oxidative stress and genotoxicity induced by glyphosate-Roundup® using zebrafish (Danio rerio) as a model. Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-018-1350-6

  • D'Costa A, Shyama SK, Praveen Kumar MK (2017) Bioaccumulation of trace metals and total petroleum and genotoxicity responses in an edible fish population as indicators of marine pollution. Ecotoxicol Environ Saf 142:22–28. https://doi.org/10.1016/j.ecoenv.2017.03.049

    Article  CAS  Google Scholar 

  • Edokpayi JN, Enitan AM, Mutileni N, Odiyo JO (2018) Evaluation of water quality and human risk assessment due to heavy metals in groundwater around Muledane area of Vhembe District, Limpopo Province, South Africa. Chem Cent J 12(2). https://doi.org/10.1186/s13065-017-0369-y

  • El Haimeur B, Bouhallaoui M, Zbiry M, Elkhiati N, Talba S, Sforzini S, Viarengo A, Benhra A (2017) Use of biomarkers to evaluate the effects of environmental stressors on Mytilus galloprovincialis sampled along the Moroccan coasts: integrating biological and chemical data. Mar Environ Res 130:60–68. https://doi.org/10.1016/j.marenvres.2017.05.010

    Article  CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem 82:70–77

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Eryılmaz O, Ateş PS, Ünal İ, Üstündağ ÜV, Bay S, Alturfan AA, Yiğitbaşı T, Emekli-Alturfan E, Akalın M (2018) Evaluation of the interaction between proliferation, oxidant-antioxidant status, Wnt pathway, and apoptosis in zebrafish embryos exposed to silver nanoparticles used in textile industry. J Biochem Mol Toxicol 32(1). https://doi.org/10.1002/jbt.22015

  • Farah SB (2007) DNA: segredos & mistério. Sarvier, São Paulo

    Google Scholar 

  • Fenech M (2007) Cytokinesis-block micronucleus cytome assay. Nat Protoc 2(5):1084–1104

    Article  CAS  Google Scholar 

  • Fenech M et al (2011) Molecular mechanisms of micronucleus, nucleoplasmic bridge and nuclear bud formation in mammalian and human cells. Mutagenesis 26:125–132. https://doi.org/10.1093/mutage/geq052

    Article  CAS  Google Scholar 

  • Foyet HS, Tchinda Deffo S, Koagne Yewo P, Antioch I, Zingue S, Asongalem EA, Kamtchouing P, Ciobica A (2017) Ficus sycomorus extract reversed behavioral impairment and brain oxidative stress induced by unpredictable chronic mild stress in rats. BMC Complement Altern Med 17(1):502. https://doi.org/10.1186/s12906-017-2012-9

    Article  CAS  Google Scholar 

  • Freitas MA, Caye BR, Machado JFL (2003) Diagnóstico dos recursos hídricos subterrâneos do oeste do estado de Santa Catarina: Projeto oeste de Santa Catarina/PROESC. CPRM/SDM-SC/SDA-SC/EPAGRI, Porto Alegre

    Google Scholar 

  • Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function and diseases. Antioxid Redox Signal 15(6):1583–1606. https://doi.org/10.1089/ars.2011.3999

    Article  CAS  Google Scholar 

  • Gabriel D, Riffel AP, Finamor IA, Saccol EM, Ourique GM, Goulart LO, Kochhann D, Cunha MA, Garcia LO, Pavanato MA, Val AL, Baldisserotto B, Llesuy SF (2013) Effects of subchronic manganese chloride exposure on tambaqui (Colossoma macropomum) tissues: oxidative stress and antioxidant defenses. Arch Environ Contam Toxicol 64(4):659–667. https://doi.org/10.1007/s00244-012-9854-4

    Article  CAS  Google Scholar 

  • Gouvea HAC, dos SLA, Cardoso FH, de SRD (2015) A relevância do tema água no ensino de ciências. Environmental Monographs Journal 14:157–171

    Google Scholar 

  • Haverroth GMB, 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 

  • Idalencio R, Kalichak F, Rosa JGS, Oliveira TA d, Koakoski G, Gusso D, Abreu MS d, Giacomini ACV, Barcellos HH d A, Piato AL, Barcellos LJG (2015) Waterborne risperidone decreases stress response in zebrafish. PLoS One 10(10):e0140800. https://doi.org/10.1371/journal.pone.0140800

    Article  CAS  Google Scholar 

  • Johnson CD, Nandi A, Joyner TA, Luffman I (2017) Iron and manganese in groundwater: using kriging and GIS to locate high concentrations in Buncombe County, North Carolina. Groundwater. https://doi.org/10.1111/gwat.12560

  • Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology. 283:65–87. https://doi.org/10.1016/j.tox.2011.03.001

    Article  CAS  Google Scholar 

  • Kaizer RR, Corrêa MC, Spanevello RM, Morsch VM, Mazzanti CM, Gonçalves JF, Schetinger MR (2005) Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminum on different mouse brain regions. J Inorg Biochem 99(9):1865–1870. https://doi.org/10.1016/j.jinorgbio.2005.06.015

    Article  CAS  Google Scholar 

  • Kar I, Mukhopadhayay SK, Patra AK, Pradhan S (2017) Bioaccumulation of selected heavy metals and histopathological and hematobiochemical alterations in backyard chickens reared in an industrial area. India Environ Sci Pollut Res Int. https://doi.org/10.1007/s11356-017-0799-z

  • Kim SH, Yadav D, Kim S, Kim JR, Cho KH (2017) High consumption of iron exacerbates hyperlipidemia, atherosclerosis, and female sterility in zebrafish via acceleration of glycation and degradation of serum lipoproteins. Nutrients. 9(7):690. https://doi.org/10.3390/nu9070690

    Article  CAS  Google Scholar 

  • Koenig JA, Dao TL, Kan RK, Shih TM (2016) Zebrafish as a model for acetylcholinesterase-inhibiting organophosphorus agent exposure and oxime reactivation. Ann N Y Acad Sci 1374(1):68–77. https://doi.org/10.1111/nyas.13051

    Article  CAS  Google Scholar 

  • Kovrižnych JA, Sotníková R, Zeljenková D, Rollerová E, Szabová E (2014) Long-term (30 days) toxicity of NiO nanoparticles for adult zebrafish Danio rerio. Interdiscip Toxicol 7(1):23–26. https://doi.org/10.2478/intox-2014-0004

    Article  CAS  Google Scholar 

  • Kumar N, Krishnani KK, Singh NP (2017) Oxidative and cellular stress as bioindicators for metal contamination in freshwater mollusk Lamellidens marginalis. Environ Sci Pollut Res Int 24(19):16137–16147. https://doi.org/10.1007/s11356-017-9266-0

    Article  CAS  Google Scholar 

  • Lawrence C, Mason T (2012) Zebrafish housing systems: a review of basic operating principles and considerations for design and functionality. ILAR J 53(2):179–191. https://doi.org/10.1093/ilar.53.2.179

    Article  CAS  Google Scholar 

  • Lionetto MG, Caricato R, Calisi A, Giordano ME, Schettino T (2013) Acetylcholinesterase as a biomarker in environmental and occupational medicine: new insights and future perspectives. Biomed Res Int. https://doi.org/10.1155/2013/321213

  • Liu Z, Shen HC, Lian TH, Mao L, Tang SX, Sun L, Huang XY, Guo P, Cao CJ, Yu SY, Zuo LJ, Wang XM, Chen SD, Chan P, Zhang W (2017) Iron deposition in substantia nigra: abnormal iron metabolism, neuroinflammatory mechanism and clinical relevance. Sci Rep 7(1):14973. https://doi.org/10.1038/s41598-017-14721-1

    Article  CAS  Google Scholar 

  • Marcon, M, Herrmann, AP, Mocelin, R Rambo, CL, Koakoski, G, Abreu, MS, Conterato, GMM, Kist, LW, Bogo, MR, Zanatta, L, Barcellos, LJG Piato, AL (2016) Prevention of unpredictable chronic stress-related phenomena in zebrafish exposed to bromazepam, fluoxetine and nortriptyline. Psychopharmacology 233(21-22):3815–3824

    Article  CAS  Google Scholar 

  • Maximino C, Benzecry R, Matos Oliveira KR, Oliveira Batista EJ, Herculano AM, Rosemberg DB, de Oliveira DL, Blaser R (2012) A comparison of the light/dark and novel tank tests in zebrafish. Behaviour. 149:1099–1123. https://doi.org/10.1163/1568539X-00003029

    Article  Google Scholar 

  • Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711–760. https://doi.org/10.1146/annurev.bi.52.070183.003431

    Article  CAS  Google Scholar 

  • Miao W, Zhu B, Xiao X, Li Y, Dirbaba NB, Zhou B, Wu H (2015) Effects of titanium dioxide nanoparticles on lead bioconcentration and toxicity on thyroid endocrine system and neuronal development in zebrafish larvae. Aquat Toxicol 161:117–126. https://doi.org/10.1016/j.aquatox.2015.02.002

    Article  CAS  Google Scholar 

  • Miranda Santos S d F d O, Hatakeyama K (2012) Processo sustentável de produção de carvão vegetal quanto aos aspectos: ambiental, econômico, social e cultural. Production. 22(2):309–321. https://doi.org/10.1590/S0103-65132012005000010

    Article  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247(10):3170–3175

    CAS  Google Scholar 

  • Mocelin R, Herrmann AP, Marcon M, Rambo CL, Rohden A, Bevilaqua F, de AMS, Zanatta L, Elisabetsky E, Barcellos LJ, Lara DR, Piato AL (2015) N-acetylcysteine prevents stress-induced anxiety behavior in zebrafish. Pharmacol Biochem Behav 139:121–166. https://doi.org/10.1016/j.pbb.2015.08.006

    Article  CAS  Google Scholar 

  • Morris G, Anderson G, Dean O, Berk M, Galecki P, Martin-Subero M, Maes M (2014) The glutathione system: a new drug target in neuroimmune disorders. Mol Neurobiol 50(3):1059–1084. https://doi.org/10.1007/s12035-014-8705-x

    Article  CAS  Google Scholar 

  • Mu X, Wang K, Chai T, Zhu L, Yang Y, Zhang J, Pang S, Wang C, Li X (2015) Sex specific response in cholesterol level in zebrafish (Danio rerio) after long-term exposure of difenoconazole. Environ Pollut 197:278–286. https://doi.org/10.1016/j.envpol.2014.11.019

    Article  CAS  Google Scholar 

  • Murray RK (2014). Bioquímica ilustrada de Harper. AMGH, Porto Alegre

  • Oliveira LCA, Fabris JD, Pereira MC (2013) Óxidos de ferro e suas aplicações em processos catalíticos: uma revisão. Quim Nova 36(1):123–130. https://doi.org/10.1590/S0100-40422013000100022

    Article  CAS  Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. https://doi.org/10.5194/hess-11-1633-2007

    Article  Google Scholar 

  • Pérez-Coyotl I, Martínez-Vieyra C, Galar-Martínez M, Gómez-Oliván LM, García-Medina S, Islas-Flores H, Pérez-Pasten Borja R, Gasca-Pérez E, Novoa-Luna KA, Dublán-García O (2017) DNA damage and cytotoxicity induced on common carp by pollutants in water from an urban reservoir. Madín reservoir, a case study. Chemosphere. 185:789–797. https://doi.org/10.1016/j.chemosphere.2017.07.072

    Article  CAS  Google Scholar 

  • Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83:346–356

    Article  CAS  Google Scholar 

  • Racette BA, Aschner M, GuilarteTR DU, Criswell SR, Zheng W (2012) Pathophysiology of manganese-associated neurotoxicity. Neurotoxicology. 3(4):881–886. https://doi.org/10.1016/j.neuro.2011.12.010

    Article  CAS  Google Scholar 

  • Radi E, Formichi P, Battisti C, Federico A (2011) Apoptosis and oxidative stress in neurodegenerative diseases. J Alzheimers Dis 42:S125–S152. https://doi.org/10.3233/JAD-132738

    Article  CAS  Google Scholar 

  • Rang HP, Dale MM, Ritter JM, Flower RJ, Henderson G (2011) Farmacologia. Elsevier, Rio de Janeiro

    Google Scholar 

  • Reddy UA, Prabhakar PV, Mahboob M (2017) Biomarkers of oxidative stress for in vivo assessment of toxicological effects of iron oxide nanoparticles. Saudi J Biol Sci 24(6):1172–1180. https://doi.org/10.1016/j.sjbs.2015.09.029

    Article  CAS  Google Scholar 

  • Romero A, Ramos E, de Los Ríos C, Egea J, Del Pino J, Reiter RJ (2014) A review of metal-catalyzed molecular damage: protection by melatonina. J Pineal Res 56(4):343–370. https://doi.org/10.1111/jpi.12132

    Article  CAS  Google Scholar 

  • Rosemberg DB, da Rocha RF, Rico EP, Zanotto-Filho A, Dias RD, Bogo MR, Bonan CD, Moreira JC, Klamt F, Souza DO (2010) Taurine prevents enhancement of acetylcholinesterase activity induced by acute ethanol exposure and decreases the level of markers of oxidative stress in zebrafish brain. Neuroscience. 171(3):683–692. https://doi.org/10.1016/j.neuroscience.2010.09.030

    Article  CAS  Google Scholar 

  • Sampaio FG, Boijink C de L, Rantin FT (2013) O uso do sulfato de cobre em ecossistemas aquáticos: Fatores que afetam sua toxicidade em peixes de água doce. Embrapa Meio Ambiente, São Paulo

    Google Scholar 

  • Sant’anna MCB, Soares V de M, Seibt KJ, Ghisleni G, Rico EP, Rosemberg DB, de OJR, Schröder N, Bonan CD, Bogo MR (2011) Iron exposure modifies acetylcholinesterase activity in zebrafish (Danio rerio) tissues: distinct susceptibility of tissues to iron overload. Fish Physiol Biochem 37(3):573–581. https://doi.org/10.1007/s10695-010-9459-7

    Article  CAS  Google Scholar 

  • Sarkar S, Mukherjee S, Chattopadhyay A, Bhattacharya S (2014) Low dose of arsenic trioxide triggers oxidative stress in zebrafish brain: expression of antioxidant genes. Ecotoxicol Environ Saf 107:1–8. https://doi.org/10.1016/j.ecoenv.2014.05.012

    Article  CAS  Google Scholar 

  • Sievers M, Hale R, Swearer SE, Parris KM (2018) Contaminant mixtures interact to impair predator-avoidance behaviours and survival in a larval amphibian. Ecotoxicol Environ Saf 14(161):482–488. https://doi.org/10.1016/j.ecoenv.2018.06.028

    Article  CAS  Google Scholar 

  • Silins I, Högberg J (2011) Combined toxic exposures and human health: biomarkers of exposure and effect. Int J Environ Res Public Health 8(3):629–647. https://doi.org/10.3390/ijerph8030629

    Article  Google Scholar 

  • Siraj M, Khisroon M, Khan A, Zaidi F, Ullah A, Rahman G (2018) Bio-monitoring of tissue accumulation and genotoxic effect of heavy metals in Cyprinus carpio from from River Kabul Khyber Pakhtunkhwa Pakistan. Bull Environ Contam Toxicol. https://doi.org/10.1007/s00128-017-2265-5

  • Spanopoulos-Zarco P, Ruelas-Inzunza J, Aramburo-Moran IS, Bojórquez-Leyva H, Páez-Osuna F (2017) Differential tissue accumulation of copper, iron, and zinc in bycatch fish from the Mexican Pacific. Biol Trace Elem Res 176(1):201–206. https://doi.org/10.1007/s12011-016-0800-6

    Article  CAS  Google Scholar 

  • Tu H, Fan C, Chen X, Liu J, Wang B, Huang Z, Zhang Y, Meng X, Zou F (2016) Effects of cadmium, manganese, and lead on locomotor activity and neurexin 2a expression in zebrafish. Environ Toxicol Chem 36(8):2147–2154. https://doi.org/10.1002/etc.3748

    Article  CAS  Google Scholar 

  • WHO (2003) Iron in drinking-water. Background document for development of WHO guidelines for drinking-water quality. World Health Organization, Geneva

    Google Scholar 

  • WHO (2004) Copper in drinking-water. Background document for development of WHO guidelines for drinking-water quality. World Health Organization, Geneva

    Google Scholar 

  • WHO (2011) Manganese in drinking-water. Background document for development of WHO guidelines for drinking-water quality. World Health Organization, Geneva

    Google Scholar 

  • Wohlenberg M, Almeida D, Bokowski L, Medeiros N, Agostini F, Funchal C, Dani C (2014) Antioxidant activity of grapevine leaf extracts against oxidative stress induced by carbon tetrachloride in cerebral cortex, hippocampus and cerebellum of rats. Antioxidants (Basel) 3(2):200–211. https://doi.org/10.3390/antiox3020200

    Article  CAS  Google Scholar 

  • Yilmaz AB, Yanar A, Alkan EN (2017) Review of heavy metal accumulation on aquatic environment in Northern East Mediterrenean Sea part I: some essential metals. Rev Environ Health 32(1–2):119–163. https://doi.org/10.1515/reveh-2016-0065

    Article  CAS  Google Scholar 

  • Zhang T, Yang M, Pan H, Li S, Ren B, Ren Z, Xing N, Qi L, Ren Q, Xu S, Song J, Ma J (2016a) Does time difference of the acetylcholinesterase (AChE) inhibition in different tissues exist? A case study of zebra fish (Danio rerio) exposed to cadmium chloride and deltamethrin. Chemosphere 168:908–916. https://doi.org/10.1016/j.chemosphere.2016.10.119

    Article  CAS  Google Scholar 

  • Zhang QF, Li YW, Liu ZH, Chen QL (2016b) Reproductive toxicity of inorganic mercury exposure in adult zebrafish: histological damage, oxidative stress, and alterations of sex hormone and gene expression in the hypothalamic-pituitary-gonadal axis. Aquat Toxicol 177:417–424. https://doi.org/10.1016/j.aquatox.2016.06.018

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We really appreciate the help provided by the company Leão Poços Artesianos to collect groundwater.

Funding

This work was supported by the Research Project Rede Guarani Serra Geral (CTHidro/ANA/CNPq/FAPESC), FAPESC/CAPES (Public Call 05/2015), PIBIC/CNPq (Notice 070/REITORIA/2016 and 040/Reitoria/2017), and Unochapecó.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed substantially to the work reported. KM and LZ conceived and designed the experiments, analyzed the data, and wrote the paper; LMVL, GB, KB, AS, MZS, RC, AL, and APZ performed the experiments; AMS and JD contributed with materials and analysis tools.

Corresponding author

Correspondence to Leila Zanatta.

Ethics declarations

The zebrafish were used and preserved according to the National Institute of Health Guide for Care and Use of Laboratory Animals. The Ethics Committee of Universidade Comunitária da Região de Chapecó (Unochapecó) approved the protocol under the number 005/2016.

Conflict of interest

The authors declare that there is no conflict of interest.

Additional information

Responsible editor: Cinta Porte

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 137 kb)

ESM 2

(PDF 88 kb)

ESM 3

(PDF 87 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Marins, K., Lazzarotto, L.M.V., Boschetti, G. et al. Iron and manganese present in underground water promote biochemical, genotoxic, and behavioral alterations in zebrafish (Danio rerio). Environ Sci Pollut Res 26, 23555–23570 (2019). https://doi.org/10.1007/s11356-019-05621-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05621-0

Keywords

Navigation