Abstract
The streams and rivers of the Upper Paraná River Basin have been seriously affected by impacts of high population density around the basin area. Fishes are widely used as models to assess the health of aquatic ecosystems, being considered as bioindicators of environmental pollution. In this context, our objective was to assess the potential genotoxic and mutagenic effects of the polluted water in three native fish species (Astyanax lacustris, Hypostomus ancistroides, and Rhamdia quelen) from Tarumã Microbasin, Upper Paraná River, Brazil. We also investigated the concentration of metals in water and in fish muscle to verify bioavailability and bioaccumulation of metals. For both less impacted sites (LI) and impacted sites (IMP) of the microbasin, the concentrations of metals were above the maximum limit allowed by Brazilian legislation (Resolution CONAMA 357/2005), except for Pb, total Cr, and Cu at LI sites and total Cr at IMP sites. A. lacustris showed a higher frequency of micronuclei (MN) at IMP sites compared with LI sites (p < 0.0001). We found no significant differences in MN frequency between site classes for H. ancistroides and R. quelen (p > 0.05). There were no significant differences between site classes regarding to nuclear abnormalities in erythrocytes frequencies (p > 0.05). A. lacustris from IMP sites had higher concentrations of Pb, Cu, Fe, Zn, and Ni in muscle tissue (p < 0.05), whereas H. ancistroides from IMP sites had higher concentration of Cr, Cu, and Ni (p < 0.0001) and R. quelen showed higher concentration of Cd, Fe, and Ni at these sites (p < 0.0001). So, the chosen biomarkers are able to identify the environmental risk of the water pollution.
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References
Adjroud O (2013) The toxic effects of nickel chloride on liver, erythropoiesis, and development in Wistar albino preimplanted rats can be reversed with selenium pretreatment. Environ Toxicol 28(5):290–298. https://doi.org/10.1002/tox.20719
Alamdar A, Eqani SA, Hanif N, Ali SM, Fasola M, Bokhari H, Katsoyiannis IA, Shen H (2017) Human exposure to trace metals and arsenic via consumption of fish from river Chenab, Pakistan and associated health risks. Chemosphere 168(1):1004–1012. https://doi.org/10.1016/j.chemosphere.2016.10.110
ANVISA (1998) Agência Nacional de Vigilância Sanitária do Brasil. Portaria n. 685, de 27 de agosto de. http://www.agricultura.gov.br. Accessed 12 Jan 2017
ANVISA (2013) Agência Nacional de Vigilância Sanitária do Brasil. Portaria n. 685, de 27 de agosto de. http://www.agricultura.gov.br. Accessed 12 Jan 2017
Arslan ÇÖ, Boyacioğlu M, Parlak H, Katalay S, Karaaslan MA (2015) Assessment of micronuclei induction in peripheral blood and gill cells of some fish species from Aliağa Bay Turkey. Mar Pollut Bull 94(1–2):48–54. https://doi.org/10.1016/j.marpolbul.2015.03.018
Batista NJ, Carvalho MCAA, Oliveira MG, Medeiros EC, Machado JL, Evangelista SR, Dias JF, Santos CE, Duarte A, Silva FR, Silva J (2016) Genotoxic and mutagenic evaluation of water samples from a river under the influence of different anthropogenic activities. Chemosphere 164(1):134–141. https://doi.org/10.1016/j.chemosphere.2016.08.091
Bednarova Z, Kuta J, Kohut L, Machat J, Klanova J, Holoubek I, Jarkovsky J, Dusek L, Hilscherova K (2013) Spatial patterns and temporal changes of heavy metal distributions in river sediments in a region with multiple pollution sources. J Soils Sedim 13(7):1257–1269. https://doi.org/10.1007/s11368-013-0706-2
Beyersmann D, Hartwig A (2008) Carcionogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82(8):493–512. https://doi.org/10.1007/s00204-008-0313-y
Bianchi E, Goldoni A, Trintinaglia L, Lessing G, Silva CEM, Nascimento CA, Ziulkoski AL, Spilki FR, Silva LB (2015) Evaluation of genotoxicity and cytotoxicity of water samples from the Sinos River Basin, southern Brazil. Braz J Biol 75(2):68–74. https://doi.org/10.1590/1519-6984.1913
Bogoni JA, Armiliato N, Araldi-Favassa CT, Techio VH (2014) Genotoxicity in Astyanax bimaculatus (Twospot Astyanax) exposed to the waters of Engano River (Brazil) as determined by micronucleus tests in erythrocytes. Arch Environ Contam Toxicol 66(3):441–449. https://doi.org/10.1007/s00244-013-9990-5
Bolognesi C, Hayashi M (2011) Micronucleus assay in aquatic animals. Mutagenesis 26(1):205–213. https://doi.org/10.1093/mutage/geq073.PMid:21164204
Bueno-Krawczyk AC, Guiloski IC, Piancini LD, Azevedo JC, Ramsdorf WA, Ide AH, Guimarães AT, Cestari MM, Silva AHC (2015) Multibiomarker in fish to evaluate a river used to water public supply. Chemosphere 135(1):257–264. https://doi.org/10.1016/j.chemosphere.2015.04.064
Camargo MMP, Martinez CBR (2006) Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil. Environ Toxicol Pharmacol 21(1):61–69. https://doi.org/10.1016/j.etap.2005.07.016
Cantanhêde SM, Silva CG, Pereira NJ, Pinho CJS, Silva J, Tchaicka L, Neta RN, Souza TJR Jr, Santos DM (2016) Evaluation of environmental quality of two estuaries in Ilha do Maranhão, Brazil, using histological and genotoxic biomarkers in Centropomus undecimalis (Pisces, Centropomidae). Environ Sci Pollut Res 23(20):21058–21069. https://doi.org/10.1007/s11356-016-7294-9
Carrasco KR, Tilbury KL, Mayers MS (1990) Assessment of the piscine micronuclei test as an in situ biological indicator of chemical contaminations effects. Can J Fish Aquaric Sci 47(11):2123–2136. https://doi.org/10.1016/j.etap.2005.07.016
Carvalho CDS, Bernusso VA, Fernandes MN (2015) Copper levels and changes in pH induce oxidative stress in the tissue of curimbata (Prochilodus lineatus). Aquat Toxicol 167(1):220–227. https://doi.org/10.1016/j.aquatox.2015.08.003
Casatti L (2002) Alimentação dos peixes em um riacho do Parque Estadual Morro do Diabo, bacia do alto Rio Paraná, sudeste do Brasil. Biot Neotropica 2(2):1–14. https://doi.org/10.1590/S1676-06032002000200012
Casatti L, Castro RMC (2006) Testing the ecomorphological hypothesis in a headwater riffles fish assemblage of the rio São Francisco, southeastern Brazil. Neotrop Ichthyol 4(2):203–214. https://doi.org/10.1590/S1679-62252006000200006
Castro BB, Sobral O, Guilhermino L, Ribeiro R (2004) An in situ biossay integrating individual and biochemical responses using small fish species. Ecotoxicology 13(7):667–681. https://doi.org/10.1007/s10646-003-4427-y
Cazenave J, Bacchetta C, Parma MJ, Scarabotti PA, Wunderlin DA (2009) Multiple biomarkers responses in Prochilodus lineatus allowed assessing changes in the water quality of Salado River basin (Santa Fe, Argentina). Environ Pollut 157(11):3025–3033. https://doi.org/10.1016/j.envpol.2009.05.055
Cheng QL, Wang RL, Huang WH, Wang WL, Li XD (2015) Assessment of heavy metal contamination in the sediments from the Yellow River Wetland National Nature Reserve (the Sanmenxia section), China. Environ Sci Pollut Res 22(11):8586–8593. https://doi.org/10.1007/s11356-014-4041-y
Colin N, Porte C, Fernandes D, Barata C, Padrós F, Carrassón M, Monroy M, Cano-Rocabayera O, Sostoa A, Piña B, Maceda-Veiga A (2016) Ecological relevance of biomarkers in monitoring studies of macro-invertebrates and fish in Mediterranean rivers. Sci Total Environ 540(1):307–323. https://doi.org/10.1016/j.scitotenv.2015.06.099
CONAMA—Conselho Nacional do Meio Ambiente (2005) Resolução n 357. Diário Oficial da União de 17 de Março de 2005. http://www.mma.gov.br/port/conama/legiabre.cfm?codlegi=459. Accessed 20 June 2014
Dalzochio T, Ressel Simões LA, Santos de Souza M, Prado Rodrigues GZ, Petry IE, Andriguetti NB, Herbert Silva GJ, Gehlen G, Basso da Silva L (2017) Water quality parameters, biomarkers and metal bioaccumulation in native fish captured in the Ilha River, Southern Brazil. Chemosphere 189:609–618. https://doi.org/10.1016/j.chemosphere.2017.09.089
Diop M, Howsam M, Diop C, Goossens JF, Diouf A, Amara R (2016) Assessment of trace element contamination and bioaccumulation in algae (Ulva lactuca), mussels (Perna perna), shrimp (Penaeus kerathurus), and fish (Mugil cephalus, Saratherondon melanotheron) along the Senegalese coast. Mar Pollut Bull 103(1–2):339–343. https://doi.org/10.1016/j.marpolbul.2015.12.038
Dourado PL, Rocha MP, Roveda LM, Raposo JL, Junior- Cândido LS, Cardoso CA, Morales MA, Oliveira KM, Grisolia AB (2016) Genotoxic and mutagenic effects of polluted surface water in the midwestern region of Brazil using animal and plant bioassays. Genet Mol Biol 40(1):123–133. https://doi.org/10.1590/1678-4685-GMB-2015-0223
Eneji IS, Shaíato R, Annune PA (2011) Bioaccumulation of Heavy Metals in Fish (Tilapia Zilli and Clarias Gariepinus) Organs from River Benue, North ñ Central Nigeria. Pak J Anal Environ Chem 12(1–2):25–31
FAO (2009) Compilation of legal limits for hazardous substance in fish and fishery products (Food and Agricultural Organization). FAO Fish Circ 464:5–100
Fenech M (2000) The in vitro micronucleus technique. Mutat Res 455(1–2):81–95. https://doi.org/10.1016/S0027-5107(00)00065-8
Fenech M, Chanq WP, Kirsch-Volders M, Holland N, Bonassi S, Zeiger E (2003) HUMN project: detailed description of the scoring criteria for the cytokinesis-block micronucleus assay using isolated human lymphocyte cultures. Mutat Rese 534(1–2):65–75. https://doi.org/10.1016/S1383-5718(02)00249-8
Ferreira AP, Horta MA, Cunha CLN (2010) Assessment of heavy metal concentrations in sediment, water and organs of Nycticorax nycticorax (Black-crowned Night Heron) in Sepetiba Bay. Rio de Janeiro, Brazil. Rev Ges Cost Int 10(2):229–241
FAO (1983) Compilation of legal limits for hazardous substances in fish and fishery products. FAO Fishery Circular 464:5–100
Gárriz Á, Del Fresno PS, Carriquiriborde P, Miranda LA (2018) Effects of heavy metals identified in Chascomús shallow lake on the endocrine- reproductive axis of pejerrey fish (Odontesthes bonariensis). Gen Comp Endocrinol S0016–6480(17):30874-2. https://doi.org/10.1016/j.ygcen.2018.06.013
Ghisi NC, Oliveira EC, Favaro LF, Silva de Assis HC, Prioli AJ (2014) In situ assessment of a neotropical fish to evaluate pollution in a river receiving agricultural and urban wastewater. Bull Environ Contam Toxicol 93(6):699–709. https://doi.org/10.1007/s00128-014-1403-6
Ghisi NC, Oliveira EC, Mendonça Mota TF, Vanzetto GV, Roque AA, Godinho JP, Bettim FL, Silva de Assis HC, Prioli AJ (2016) Integrated biomarker response in catfish Hypostomus ancistroides by multivariate analysis in the Pirapó River, southern Brazil. Chemosphere 161(1):69–79. https://doi.org/10.1016/j.chemosphere.2016.06.113
Gomiero LM, Souza UP, Braga FMS (2007) Reproduction and feeding of Rhamdia quelen (Quoy & gaimard, 1824) in rivers of the Santa Virgínia unit, State park of the Serra do Mar, São Paulo SP. Biot. Neotrop 7(3):127–133. https://doi.org/10.1590/S1676-06032007000300015
Grisolia CK, Rivero CLG, Starling FLRM, Da Silva ICR, Barbosa AC, Dorea JG (2009) Profle of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genet Mol Biol 32(1):138–143. https://doi.org/10.1590/S1415-47572009005000009
Gutiérrez JM, Villar S, Plavan AA (2015) Micronucleus test in fshes as indicators of environmental quality in subestuaries of the Río de la Plata (Uruguay). Mar Pollut Bull 91(2):518–523. https://doi.org/10.1016/j.marpolbul.2014.10.027
Hemachandra CK, Pathiratne A (2016) Combination of physico-chemical analysis, Allium cepa test system and Oreochromis niloticus erythrocyte based comet assay/nuclear abnormalities tests for cyto-genotoxicity assessments of treated effluents discharged from textile industries. Ecotox Environ Saf 131(1):54–64. https://doi.org/10.1016/j.ecoenv.2016.05.010
Jesus IS, Cestari MM, Bezerra MA, Mello Affonso PR (2016) Genotoxicity effects in freshwater fish from a Brazilian impacted river. Bull Environ Contam Toxicol 96(4):490–495. https://doi.org/10.1007/s00128-016-1755-1
Kubrak OI, Husak VV, Rovenko BM, Poigner H, Kriews M, Abele D, Lushchak VI (2013) Antioxidant system efficiently protects goldfish gills from Ni2-induced oxidative stress. Chemosphere 90(3):971–976. https://doi.org/10.1016/j.chemosphere.2012.06.044
Lavado R, Urena R, Martin-Skilton R, Torreblanca A, Del Ramo J, Raldúa D, Porte C (2006) The combined use of chemical and biochemical markers to assess water quality along the Ebro River. Environ Pollut 139(2):330–339. https://doi.org/10.1016/j.envpol.2005.05.003
Leung HM, Leung AOW, Wang HS, Ma KK, Liang Y, Ho KC, Cheung KC, Tohidi F, Yung KKL (2014) Assessment of heavy metals/metalloid (As, Pb, Cd, Ni, Zn, Cr, Cu and Mn) concentrations in edible fish species tissue in the Pearl River Delta (PRD), China. Mar Pollut Bull 78(1–2):235–245. https://doi.org/10.1016/j.marpolbul.2013.10.028
Lopes C, Herva M, Franco-Uría M, Roca E (2011) Inventory of heavy metal content in organic waste applied as fertilizer in agriculture: evaluating the risk of transfer into the food chain. Environ Sci Poll Res 18(6):918–939. https://doi.org/10.1007/s11356-011-0444-1
Monaco IA, Súarez YR, Lima-Junior SE (2014) Infuence of environmental integrity on feeding, condition and reproduction of Phalloceros harpagos Lucinda, 2008 in the Tarumã stream microbasin. Acta Sci Biol Sci 36(2):181–188. https://doi.org/10.4025/actascibiolsci.v36i2.21394
Obiakor MO, Okonkwo JC, Ezeonyejiaku CD (2014) Genotoxicity of freshwater ecosystem shows DNA damage in preponderant fish as validated by in vivo micronucleus induction in gill and kidney erythrocytes. Mutat Res Gen Tox 775(1):20–30. https://doi.org/10.1016/j.mrgentox.2014.09.010
Omar WA, Zaghloul KH, Abdel-Khalek AA, Abo-Hegab S (2012) Genotoxic effects of metal pollution in two fish species, Oreochromis niloticus and Mugil cephalus, from highly degraded aquatic habitats. Mutat Res 746(1):7–14. https://doi.org/10.1016/j.mrgentox.2012.01.013
Ossana NA, Eissa BL, Baudou FG, Castañé PM, Soloneski S, Ferrari L (2016) Multibiomarker response in ten spotted live-bearer fish Cnesterodon decemmaculatus (Jenyns, 1842) exposed to Reconquista river water. Ecotoxicol Environ Saf 133(1):73–81. https://doi.org/10.1016/j.ecoenv.2016.06.046
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
Schmid W (1975) The micronucleus test. Mutat Res 31:9–15
Seixas TG, Kehrig HA, Di Beneditto AP, Souza CM, Malm O, Moreira I (2009) Essential (Se and Cu) and non-essential (Ag, Hg and Cd) elements: what are their relationships in liver of Sotalia guianensis (Cetacea, Delphinidae)? Mar Pollut Bull 58(4):629–634. https://doi.org/10.1016/j.marpolbul.2008.12.005
Silva VSS, Dias AH, Dutra ES, Pavanin AL, Morelli S, Pereira BB (2015) The impact of water pollution on fish species in southeast region of Goiás, Brazil. J Tox Environ Health 79(1):8–16. https://doi.org/10.1080/15287394.2015.1099484
Silva YJAB, Cantalice JRB, Nascimento CWA, Singh VP, Silva YJAB, Silva CMCAC, Silva MO, Guerra SMS (2017) Bedload as an indicator of heavy metal contamination in a Brazilian anthropized watershed. CATENA 153(2):106–113. https://doi.org/10.1016/j.catena.2017.02.004
Simonato JD, Mela M, Doria HB, Guiloski IC, Carvalho PS, Meletti PC, Silva de Assis HC, Bianchini A, Martinez CB (2016) Biomarkers of waterborne copper exposure in the Neotropical fish Prochilodus lineatus. Aquat Toxicol 170(1):31–41. https://doi.org/10.1016/j.aquatox.2015.11.012
Siqueira-Silva DH, Silva APS, Ninhaus-Silveira A, Veríssimo Silveira R (2015) Morphology of the urogenital papilla and its components ducts in Astyanax altiparanae Garutti and Britski, 2000 (Characiformes: Characidae). Neotrop Ichthyol 13(2):309–316. https://doi.org/10.1590/1982-0224-20140102
Sofia SH, Galindo Bruno A, Paula FM, Sodré LMK, Martinez CBR (2008) Genetic diversity of Hypostomus ancistroides (Teleostei, Loricariidae) from an urban stream. Genet Mol Biol 31(1):317–323. https://doi.org/10.1590/S1415-47572008000200027
Souza RG, Lima-Junior SE (2013) Influence of environmental quality on the diet of Astyanax in a microbasin of central western Brazil. Acta Sci Biol Sci 35(2):179–184. https://doi.org/10.4025/actascibiolsci.v35i2.15570
Tabet M, Abda A, Benouareth DE, Liman R, Konuk M, Khallef M, Taher A (2015) Mutagenic and genotoxic effects of Guelma’s urban wastewater, Algeria. Environ Monit Assess 187(2):13–26. https://doi.org/10.1007/s10661-015-4281-4
Tang W, Duan S, Shan B, Zhang H, Zhang W, Zhao Y, Zhang C (2016) Concentrations, diffusive fluxes and toxicity of heavy metals in pore water of the Fuyang River, Haihe Basin. Ecotoxicol Environ Saf 127(1):80–86. https://doi.org/10.1016/j.ecoenv.2016.01.013
Topal A, Atamanalp M, Oruç E, Erol HS (2017) Physiological and biochemical effects of nickel on rainbow trout (Oncorhynchus mykiss) tissues: assessment of nuclear factor kappa B activation, oxidative stress and histopathological changes. Chemosphere 166(1):445–452. https://doi.org/10.1016/j.chemosphere.2016.09.106
Viana LF, Súarez YR, Lima-Junior SE (2013) Influence of environmental integrity on the feeding biology of Astyanax altiparanae Garutti & Britski, 2000 in the Ivinhema River Basin. Acta Sci Biol Sci 35(4):541–548. https://doi.org/10.4025/actascibiolsci.v35i4.19497
Viana LF, Súarez YR, Cardoso CAL, Solórzano JCJ, Crispim BDA, Grisolia AB, Lima-Junior SE (2017) Erythrocyte nuclear abnormalities in Astyanax lacustris in response to landscape characteristics in two neotropical streams. Arch Environ Contam Toxicol 17(1):1–8. https://doi.org/10.1007/s00244-017-0476-8
Vieira CED, Costa PG, Lunardelli B, Oliveira LF, Cabrera LC, Risso WE, Primel EG, Meletti PC, Fillmann G, Martinez CBR (2016) Multiple biomarker responses in Prochilodus lineatus subjected to short-term in situ exposure to streams from agricultural areas in Southern Brazil. Sci Technol Environ 542(1):44–56. https://doi.org/10.1016/j.scitotenv.2015.10.071
Villares Junior GA, Goitein R (2013) Differences in the feeding of Rhamdia quelen (Siluriformes, Heptapteridae) in four distinct lotic systems. Braz J Biol 75(3):650–654. https://doi.org/10.1590/1519-6984.20313
Wei Y, Zhang J, Zhang D, Tu T, Luo L (2014) Metal concentrations in various fish organs of different fish species from Poyang Lake, China. Ecotoxicol Environ Saf 104(1):182–188. https://doi.org/10.1016/j.ecoenv.2014.03.001
WHO (2003a) Iron in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/WSH/03.04/08)
WHO (2003b) Zinc in drinking-water. Background document for preparation of WHO Guidelines for drinking-water quality. Geneva, World Health Organization (WHO/SDE/WSH/03.04/17)
WHO (2009) Heavy metals-environmental aspects. Environment Health Criteria. No. 85. Geneva, Switzerland
WHO (2011) World Health Organization. Guidelines for drinking-water quality. 4th ed. WHO Library Cataloguing-in-Publication Data
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The authors thank to Grupo de Estudos em Proteção à Biodiversiade (Gebio), Ministério Público de Mato Grosso do Sul (MP-MS), Municipality of Naviraí and Polícia Militar Ambiental (PMA) for the support. They also thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) and Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (Fundect) for the scholarship to the first author and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for productivity grants to Yzel Rondon Súarez and Claudia Andréa Lima Cardoso.
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Viana, L.F., Súarez, Y.R., Cardoso, C.A.L. et al. The Response of Neotropical Fish Species (Brazil) on the Water Pollution: Metal Bioaccumulation and Genotoxicity. Arch Environ Contam Toxicol 75, 476–485 (2018). https://doi.org/10.1007/s00244-018-0551-9
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DOI: https://doi.org/10.1007/s00244-018-0551-9