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In Situ Assessment of a Neotropical Fish to Evaluate Pollution in a River Receiving Agricultural and Urban Wastewater

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Abstract

We aimed to assess the quality of a midsize river that receives agricultural and urban wastewater. Nuclear abnormalities (NA), comet assays of blood and gills, and gill histopathology were evaluated in fish Astyanax aff. paranae during the summer and winter 2011 at three sites in Paraná State, Brazil: (1) a biological reserve (Rebio—reference area); (2) an agricultural site; (3) a downstream site that accumulates agricultural and urban effluents. We found the highest effects of pollutants in fish at the downstream site during the summer. The agricultural site showed an intermediate damage rate, and fish at Rebio generally had the least damage, with the exception of NA. Despite conflicting results from the biomarkers used, we observed an increase in damage associated with the accumulation of pollutants. Pesticides are probable xenobiotics in the agricultural area. Additionally, metals and substances such as pharmaceuticals and ammonia may be present at the downstream site.

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References

  • Abdel-Moneim AM, Al-Kahtani MA, Elmenshawy OM (2012) Histopathological biomarkers in gills and liver of Oreochromis niloticus from polluted wetland environments, Saudi Arabia. Chemosphere 88:1028–1035. doi:10.1016/j.chemosphere.2012.04.001

    Article  CAS  Google Scholar 

  • Agostinho AA, Gomes LC, Pelicice FM (2007) Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil, 1st edn. EDUEM, Maringá

    Google Scholar 

  • Alberto A, Camargo AFM, Verani JR et al (2005) Health variables and gill morphology in the tropical fish Astyanax fasciatus from a sewage-contaminated river. Ecotoxicol Environ Saf 61:247–255. doi:10.1016/j.ecoenv.2004.08.009

    Article  CAS  Google Scholar 

  • Alberts B, Johnson A, Lewis J et al (2002) Molecular biology of the cell, 4th edn. Garland, New York

    Google Scholar 

  • Ali D, Nagpure NS, Kumar S et al (2009) Assessment of genotoxic and mutagenic effects of chlorpyrifos in freshwater fish Channa punctatus (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Food Chem Toxicol 47:650–656. doi:10.1016/j.fct.2008.12.021

    Article  CAS  Google Scholar 

  • Amorim LCA (2003) Os biomarcadores e sua aplicação na avaliação da exposição aos agentes químicos ambientais. Rev Bras Epidemiol 6:158–170

    Article  Google Scholar 

  • Arellano JM, Storch V, Sarasquete C (1999) Histological Changes and Copper Accumulation in Liver and Gills of the Senegales Sole, Solea senegalensis. Ecotoxicol Environ Saf 72:62–72

    Article  Google Scholar 

  • Armas E, Monteiro R, Amâncio A et al (2005) Uso de Agrotóxicos em Cana-de-Açúcar na Bacia do Rio Corumbataí e o Risco de Poluição Hídrica. Quim Nova 28:975–982

    Article  Google Scholar 

  • Ateeq B, Abul farah M, Niamat Ali M, Ahmad W (2002) Induction of micronuclei and erythrocyte alterations in the catfish Clarias batrachus by 2,4-dichlorophenoxyacetic acid and butachlor. Mutat Res 518:135–144

    Article  CAS  Google Scholar 

  • Azevedo JDS, Braga EDS, de Ribeiro CAO (2012) Nuclear abnormalities in erythrocytes and morphometic index in the Catfish Cathorops spixii (Ariidae) from different sites on the southeastern Brazilian coast. Brazilian J Oceanogr 60:323–330

    Article  Google Scholar 

  • Azevedo JS, Braga ES, Silva de Assis HC, Ribeiro CAO (2013) Biochemical changes in the liver and gill of Cathorops spixii collected seasonally in two Brazilian estuaries under varying in fl uences of anthropogenic activities. Ecotoxicol Environ Saf 96:220–230. doi:10.1016/j.ecoenv.2013.06.021

    Article  CAS  Google Scholar 

  • Bálint T, Szegletes T, Szegletesb Z et al (1995) Biochemical and subcellular changes in carp exposed to the organophosphorus methidathion and the pyrethroid deltamethrin. Aquat Toxicol 33:279–295

    Article  Google Scholar 

  • Barbieri GM (1992) Biologia de Astyanax scabripinnis paranae (Characiformes, Characidade) do ribeirão do Fazzari. São Carlos. Estado de São Paulo. II. Aspectos quantitativos da reprodução. Rev Bras Biol 52:589–596

    Google Scholar 

  • Bernet D, Schmidt H, Meier W, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess aquatic pollution. J Fish Dis 22:25–34

    Article  Google Scholar 

  • Bolognesi C, Hayashi M (2011) Micronucleus assay in aquatic animals. Mutagenesis 26:205–213. doi:10.1093/mutage/geq073

    Article  CAS  Google Scholar 

  • Brasil (2000) Law n. 9985, June 18th 2000. SNUC. 18

  • Brasil (2005) Resolução do Conselho Nacional do Meio Ambiente no. 357, de 17 de março de 2005. 1–23

  • Bucher F, Hofer R (1993) The effects of treated domestic sewage on three organs (Gills, Kidney, Liver) of Brown trout (Salmo trutta). Water Res 27:255–261

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Carrasco-Letelier L, Eguren G, de Mello FT, Groves PA (2006) Preliminary field study of hepatic porphyrin profiles of Astyanax fasciatus (Teleostei, Characiformes) to define anthropogenic pollution. Chemosphere 62:1245–1252. doi:10.1016/j.chemosphere.2005.07.005

    Article  CAS  Google Scholar 

  • Castella PR, Britez RM (2004) A floresta com araucária no Paraná: conservação e diagnóstico dos remanescentes florestais. 236

  • Çavas T (2011) In vivo genotoxicity evaluation of atrazine and atrazine-based herbicide on fish Carassius auratus using the micronucleus test and the comet assay. Food Chem Toxicol 49:1431–1435. doi:10.1016/j.fct.2011.03.038

    Article  Google Scholar 

  • Çavas T, Ergene-Gözükara S (2005a) Micronucleus test in fish cells: a bioassay for in situ monitoring of genotoxic pollution in the marine environment. Environ Mol Mutagen 46:64–70. doi:10.1002/em.20130

    Article  Google Scholar 

  • Çavas T, Ergene-Gözükara S (2005b) Induction of micronuclei and nuclear abnormalities in Oreochromis niloticus following exposure to petroleum refinery and chromium processing plant effluents. Aquat Toxicol 74:264–271. doi:10.1016/j.aquatox.2005.06.001

    Article  Google Scholar 

  • Çavas T, Könen S (2007) Detection of cytogenetic and DNA damage in peripheral erythrocytes of goldfish (Carassius auratus) exposed to a glyphosate formulation using the micronucleus test and the comet assay. Mutagenesis 22:263–268. doi:10.1093/mutage/gem012

    Article  Google Scholar 

  • Çavas T, Garanko NN, Arkhipchuk VV (2005) Induction of micronuclei and binuclei in blood, gill and liver cells of fishes subchronically exposed to cadmium chloride and copper sulphate. Food Chem Toxicol 43:569–574. doi:10.1016/j.fct.2004.12.014

    Article  Google Scholar 

  • de Andrade Brito I, Freire CA, Yamamoto FY et al (2012) Monitoring water quality in reservoirs for human supply through multi-biomarker evaluation in tropical fish. J Environ Monit JEM 14:615–625. doi:10.1039/c2em10461j

    Article  Google Scholar 

  • Fanta E, Rios FSA, Romão S et al (2003) Histopathology of the fish Corydoras paleatus contaminated with sublethal levels of organophosphorus in water and food. Ecotoxicol Environ Saf 54:119–130

    Article  CAS  Google Scholar 

  • Farah MA, Ateeq B, Ali MN, Ahmad W (2003) Evaluation of genotoxicity of PCP and 2,4-D by micronucleus test in freshwater fish Channa punctatus. Ecotoxicol Environ Saf 54:25–29. doi:10.1016/S0147-6513(02)00037-4

    Article  CAS  Google Scholar 

  • Fenech M (2007) Cytokinesis-block micronucleus cytome assay. Nat Protoc 2:1084–1104. doi:10.1038/nprot.2007.77

    Article  CAS  Google Scholar 

  • Fernandes TCC, Mazzeo DEC, Marin-Morales MA (2007) Mechanism of micronuclei formation in polyploidizated cells of Allium cepa exposed to trifluralin herbicide. Pestic Biochem Physiol 88:252–259. doi:10.1016/j.pestbp.2006.12.003

    Article  CAS  Google Scholar 

  • Fernandez WS, Dias JF, Ribeiro CAO, Azevedo JDS (2011) Liver damages and nuclear abnormalities in erythrocytes of Atherinella brasiliensis (Actynopterigii, Atherinopsidade) from two beaches in southeast of Brazil. Braz J Med Biol Res 59:163–169

    Google Scholar 

  • Ferraro MVM, Fenocchio AS, Mantovani MS et al (2004) Mutagenic effects of tributyltin and inorganic lead (Pb II) on the fish H. malabaricus as evaluated using the comet assay and the piscine micronucleus and chromosome aberration tests. Genet Mol Biol 27:103–107

    Article  CAS  Google Scholar 

  • Flammarion P, Devaux A, Nehls S et al (2002) Multibiomarker responses in fish from the Moselle river (France). Ecotoxicol Environ Saf 51:145–153. doi:10.1006/eesa.2001.2134

    Article  CAS  Google Scholar 

  • Frenzilli G, Nigro M, Lyons BP (2009) The Comet assay for the evaluation of genotoxic impact in aquatic environments. Mutat Res 681:80–92. doi:10.1016/j.mrrev.2008.03.001

    Article  CAS  Google Scholar 

  • Garutti V, Britski HA (2000) Descrição de uma espécie nova de Astyanax (Teleostei: Characidae) da bacia do alto rio Paraná e considerações sobre as demais espécies do gênero na bacia. Comun do Mus Ciências e Tecnol da PUCRS- Série Zoológica 14:65–88

    Google Scholar 

  • Guerreiro RL, Parolin M (2008) Espécies Nativas de Cerrado na Cidade de Campo Mourão: potencial para Recuperação? I Simpósio de Estudos Urbanos: desenvolvimento regional e dinâmica ambiental p 16

  • Gust M, Fortier M, Garric J et al (2013) Effects of short-term exposure to environmentally relevant concentrations of different pharmaceutical mixtures on the immune response of the pond snail Lymnaea stagnalis. Sci Total Environ 445–446:210–218. doi:10.1016/j.scitotenv.2012.12.057

    Article  Google Scholar 

  • Heddle JA (1973) A rapid in vivo test for chromosomal damage. Mutat Res 18:187–190

    Article  CAS  Google Scholar 

  • Instituto Chico Mendes I (2012) Plano de Manejo da Reserva Biológica das Perobas. 199

  • Jiraungkoorskul W, Upatham ES, Kruatrachue M et al (2003) Biochemical and histopathological effects of glyphosate herbicide on Nile Tilapia (Oreochromis niloticus). Environ Toxicol 4:260–267. doi:10.1002/tox.10123

    Article  Google Scholar 

  • Kobayashi H, Sugiyama C, Morikawa Y et al (1995) A comparison between manual microscopic analysis and computerized image analysis in the single cell gel electrophoresis. Mamm Mutagen Study Gr Commun 3:103–115

    CAS  Google Scholar 

  • Lee RF, Steinert S (2003) Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutat Res Mutat Res 544:43–64. doi:10.1016/S1383-5742(03)00017-6

    Article  CAS  Google Scholar 

  • Maack R (1981) Geografia física do Estado do Paraná, 2nd ed. 450p

  • Mallatt J (1985) Fish Gills structural changes inducted by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42:630–648

    Article  CAS  Google Scholar 

  • Marc J, Mulner-Lorillon O, Bellé R (2004) Glyphosate-based pesticides affect cell cycle regulation. Biol Cell 96:245–249. doi:10.1016/j.biolcel.2003.11.010

    Article  CAS  Google Scholar 

  • Martinez BR, Souza MM (2002) Acute effects of nitrite on ion regulation in two neotropical fish species. Comp Biochem Physiol Part A 133:151–160

    Article  Google Scholar 

  • Mela M, Guiloski IC, Doria HB et al (2013) Effects of the herbicide atrazine in neotropical cat fish (Rhamdia quelen). Ecotoxicol Environ Saf 93:13–21. doi:10.1016/j.ecoenv.2013.03.026

    Article  CAS  Google Scholar 

  • Mizote LTM (2008) Agenda 21 Local de Campo Mourão: do projeto ao processo. 238

  • Moore MN, Simpson MC (1992) Molecular and celular pathology in environmental impact assessment. Aquat Toxicol 22:313–322

    Article  CAS  Google Scholar 

  • Narain AS, Srivastava AK, Singh BB (1990) Gill Lesions in the Perch, Anabas testudineus, subjected to sewage toxicity. Bull Environ Contam Toxicol 45:235–242

    Article  CAS  Google Scholar 

  • Nero V, Farwell A, Lister A et al (2006) Gill and liver histopathological changes in yellow perch (Perca flavescens) and goldfish (Carassius auratus) exposed to oil sands process-affected water. Ecotoxicol Environ Saf 63:365–377. doi:10.1016/j.ecoenv.2005.04.014

    Article  CAS  Google Scholar 

  • Pacheco M, Santos MA (2002) Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol Environ Saf 53:331–347

    Article  CAS  Google Scholar 

  • Pane EF, Haque A, Wood CM (2004) Mechanistic analysis of acute, Ni-induced respiratory toxicity in the rainbow trout (Oncorhynchus mykiss): an exclusively branchial phenomenon. Aquat Toxicol 69:11–24. doi:10.1016/j.aquatox.2004.04.009

    Article  CAS  Google Scholar 

  • Paraná (2005) Plano de Manejo do Parque Estadual do Lago Azul. Encarte II: 1–45. Available in: http://www.iap.pr.gov.br/arquivos/File/Plano_de_Manejo/Parque_Estadual_Lago_Azul/4_PELA_ENCARTE_II.pdf. Accessed 20 jan 2014

  • Paraná (2010) Capítulo 1- Dimensão Ambiental. In: IPARDES (ed) Indicadores Ambient. por bacias hidrográficas do Estado do Paraná. Instituto Paranaense de Desenvolvimento Econômico e Social, Curitiba, p 223

  • Pereira S, Pinto AL, Cortes R et al (2013) Gill histopathological and oxidative stress evaluation in native fish captured in Portuguese northwestern rivers. Ecotoxicol Environ Saf 90:157–166. doi:10.1016/j.ecoenv.2012.12.023

    Article  CAS  Google Scholar 

  • Prioli SMAP, Prioli AJ, Júlio HF Jr et al (2002) Identification of Astyanax altiparanae (Teleostei, Characidae) in the Iguaçu River, Brazil, based on mitochondrial DNA and RAPD markers. Genet Mol Biol 430:421–430

    Article  Google Scholar 

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

  • Rossi SC, Piancini LDS, Ribeiro CAO et al (2011) Sublethal effects of waterborne herbicides in tropical freshwater fish. Bull Environ Contam Toxicol 87:603–607. doi:10.1007/s00128-011-0397-6

    Article  CAS  Google Scholar 

  • Rouimi P, Zucchini-Pascal N, Dupont G et al (2012) Impacts of low doses of pesticide mixtures on liver cell defence systems. Toxicol In Vitro 26:718–726. doi:10.1016/j.tiv.2012.03.015

    Article  CAS  Google Scholar 

  • Rybakovas A, Barsiene J, Lang T (2009) Environmental genotoxicity and cytotoxicity in the offshore zones of the Baltic and the North Seas. Mar Environ Res 68:246–256. doi:10.1016/j.marenvres.2009.06.014

    Article  CAS  Google Scholar 

  • Schmid W (1975) The micronucleus test. Mutat Res 31:9–15

    Article  CAS  Google Scholar 

  • Sharma S, Vig AP (2012) Genotoxicity of Atrazine, Avenoxan, Diuron and Quizalofop-P-ethyl Herbicides using the Allium cepa Root Chromosomal Aberration Assay. Terr Aquat Environ Toxicol 6:90–95

    Google Scholar 

  • Silva JRR, Filho HO (2011) Dípteros ectoparasitas (Insecta, Diptera) em morcegos (Chiroptera, Mammalia) na Reserva Biológica das Perobas Paraná, Brasil. Iheringia, Sér Zool 101:220–224

    Article  Google Scholar 

  • Silva de Assis HC, Simmons DBD, Zamora JM et al (2013) Estrogen-like effects in male gold fish Co-exposed to fluoxetine and. Environ Sci Technol 47:5372–5382

    Article  CAS  Google Scholar 

  • Silva HC, Medina HSG, Fanta E, Bacilat M (1993) Sub-Lethal effect of the Organophosphate Folidol 600 (Methyl Parathion) on Callichthys callichthys (Pisces: Teleostei). Comp Biochem Physiol 105C:197–201

    Google Scholar 

  • Silva MD, Rossi SC, Ghisi NDC et al (2014) Using multibiomarker approach as a tool to improve the management plan for a Private Reserve of Natural Heritage (RPPN). Bull Environ Contam Toxicol 92:602–608. doi:10.1007/s00128-014-1230-9

    Article  Google Scholar 

  • Speit G, Hartmann A (1999) The comet assay (single-cell gel test), a sensitive genotoxicity test for the detection of DNA damage and repair. In: Henderson DS (ed) Methods mol. biol. DNA repair protoc—eukaryot syst, 113th edn. Human Press, Totowa, pp 203–211

    Google Scholar 

  • Suzuki H, Agostinho AA, Winemiller KO (2000) Relationship between oocyte morphology and reproductive strategy in loricariid catfishes of the Paraná River, Brazil. J Fish Biol 57:791–807. doi:10.1006/jfbi.2000.1352

    Google Scholar 

  • Suzuki HI, Vazzoler AEAM, Marques EE, et al. (2004) Reproductive ecology of the fish assemblage. Up. Parana River its floodplain Phys. Asp. Ecol. Conserv

  • Talapatra SN, Banerjee SK (2007) Detection of micronucleus and abnormal nucleus in erythrocytes from the gill and kidney of Labeo bata cultivated in sewage-fed fish farms. Food Chem Toxicol 45:210–215. doi:10.1016/j.fct.2006.07.022

    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 

  • Von Sonntag C (1987) The chemical basis of radiation biology. 515

  • Von Sperling M (1996) Princípios básicos do tratamento de esgotos—Princípios do tratamento biológico de águas residuárias, 2nd ed. 211

  • Wirzinger G, Weltje L, Gercken J, Sordyl H (2007) Genotoxic damage in field-collected three-spined sticklebacks (Gasterosteus aculeatus L.): a suitable biomonitoring tool? Mutat Res 628:19–30. doi:10.1016/j.mrgentox.2006.11.011

    Article  CAS  Google Scholar 

  • Xie Z, Cai Y, Chen G et al (2004) Induction of micronuclei and nuclear anomalies in erythrocytes of Misgurnus anguillicaudatus by herbicide acetochlor. Fish Sci 23:17–19

    Google Scholar 

  • Zhang Y, Wang Y, Yu R et al (2008) Effects of heavy metals Cd2 +, Pb2 + and Zn2 + on DNA damage of loach Misgurnus anguillicaudatus. Front Biol China 3:50–54. doi:10.1007/s11515-008-0012-3

    Article  Google Scholar 

  • Zhou Q, Zhang J, Fu J et al (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150. doi:10.1016/j.aca.2007.11.018

    Article  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge the logistical support from the Chico Mendes Institute for Biodiversity Conservation of the Reserve of Perobas; to Nupélia (Limnology, Ichthyology and Aquiculture Research Center/UEM); to financial support from the Araucaria Foundation and SETI (Parana State Agency for Science and Technology) and to CAPES (PROEX - Brazilian Agency for Science and Technology). We greatly thank Jeffrey D. Muehlbauer for English language revisions. Voucher specimens of collected individuals were stored at the Ichthyological Collection of the Limnology, Ichthyology and Aquiculture Research Center: the JP and MP fishes NUP 13381 and Field: NCG2011103101 and the Rebio fishes NUP13382 and Field NCG2011071701.

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Ghisi, N.C., de Oliveira, E.C., Fávaro, L.F. et al. In Situ Assessment of a Neotropical Fish to Evaluate Pollution in a River Receiving Agricultural and Urban Wastewater. Bull Environ Contam Toxicol 93, 699–709 (2014). https://doi.org/10.1007/s00128-014-1403-6

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