Environmental Science and Pollution Research

, Volume 25, Issue 10, pp 9485–9500 | Cite as

In situ monitoring of the Sinos River, southern Brazil: water quality parameters, biomarkers, and metal bioaccumulation in fish

  • Thaís Dalzochio
  • Gabriela Zimmermann Prado Rodrigues
  • Leonardo Airton Ressel Simões
  • Mateus Santos de Souza
  • Ismael Evandro Petry
  • Natália Bordin Andriguetti
  • Gláucia Joselaine Herbert Silva
  • Luciano Basso da Silva
  • Günther Gehlen
Research Article


The Sinos River is an important water supply in Southern Brazil and receives industrial, agricultural, and domestic effluents which may affect aquatic biota. Water physicochemical and microbiological analyses, biomarker responses (scaled mass index (SMI), gill histopathology, and micronucleus and nuclear abnormality (MN and NA) frequencies), and metal bioaccumulation in muscle were assessed in the fish species Bryconamericus iheringii (Characidae) captured at three sampling sites (S1, S2, and S3) in four sampling periods. The mean values of five parameters (total phosphorus, thermotolerant coliforms, aluminum, iron, and lead) exceeded the limits established by the Brazilian legislation at the three sampling sites. Although physicochemical analysis indicated higher impacts at S3, in some samples, significantly higher MN frequencies and bioaccumulation of manganese in fish muscle were observed at S1, whereas low SMI and higher concentrations of aluminum and zinc in fish muscle were found at S2. Histopathological alterations in gills were observed in fish collected at the three sampling sites; however, no spatial differences were observed, indicating similar environmental conditions with respect to this biomarker. Moreover, temporal variation of biomarker responses and metal bioaccumulation were found at all sampling sites. Furthermore, the consumption of fish from the Sinos River should be avoided given the concentrations of chromium (all samples), cadmium, and lead in fish muscle above the threshold for safe human consumption.


Bioaccumulation Biomarkers Biomonitoring Pollution Sinos River 



This work was supported by the Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul—FAPERGS (scholarships), Universidade Feevale, and Conselho Nacional de Desenvolvimento Científico e Tecnólogico (CNPq) (grant number 459718/2014-2). LBS is a CNPq researcher (308244/2015-0).

Compliance with ethical standards

The procedures followed animal care protocols, and the study was approved by the Ethics Committee for Animal Experimentation of Universidade Feevale (protocol no. 02.13.022), whereas fish collections were authorized by the Brazilian environmental agency (SISBIO No. 40376–2)


  1. Adam SM (2002) Biological indicators of aquatic ecosystem stress. American Fisheries Society, Bethesda, p 656Google Scholar
  2. Adhikari S, Ghosh L, Rai SP, Ayyappan S (2009) Metal concentrations in water, sediment, and fish from sewage-fed aquaculture ponds of Kolkata, India. Environ Monit Assess 159(1-4):217–230. CrossRefGoogle Scholar
  3. Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta 1519(1):37–48CrossRefGoogle Scholar
  4. Alloway BJ (2013) Heavy metals in soils. Trace metals and metalloids in soils and their bioavailability. Environ Poll 22. Netherlands: Springer NetherlandsGoogle Scholar
  5. Al-Sabti K, Metcalfe C (1995) Fish micronuclei for assessing genotoxicity in water. Mutat Res 343(2-3):121–135. CrossRefGoogle Scholar
  6. American Public Health Association – APHA (2005) Standard methods for the examination of water and wastewater. 21st ed. Washington, D.C.Google Scholar
  7. Ameur WB, El Megdiche Y, Lapuente J, Barhoumi B, Trabelsi S, Ennaceur S, Camps L, Serret J, López DR, Linares JG, Touil S, Driss MR, Borràs M (2015) Oxidative stress, genotoxicity and histopathology biomarker responses in Mugil cephalus and Dicentrarchus labrax gill exposed to persistent pollutants. A field study in the Bizerte Lagoon: Tunisia. Chemosphere 135:67–74. CrossRefGoogle Scholar
  8. Ameur WB, Lapuente J, Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Driss MR, Borràs M (2012) Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull 64(2):241–251. CrossRefGoogle Scholar
  9. ANVISA – Agência Nacional de Vigilância Sanitária (1998) Portaria n°685, de 27 de agosto de 1998. Accessed 20 October 2016
  10. ANVISA – Agência Nacional de Vigilância Sanitária (2003) Resolução RDC n° 42, de 29 de agosto de 2013.>. Accessed 17 November 2016
  11. Asuquo FE, Ewa-Oboho I, Ausquo EF, Udo PJ (2004) Fish species used as biomarker for heavy metal and hydrocarbon contamination for Cross River, Nigeria. Environmentalist 2:29–37CrossRefGoogle Scholar
  12. Ayllón F, Garcia-Vazquez E (2000) Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: an assessment of the fish micronucleus test. Mutat Res 467(2):177–186. CrossRefGoogle Scholar
  13. Benvenuti T, Kieling-Rubio MA, Klauck CR, Rodrigues MAS (2015) Evaluation of water quality at the source of streams of the Sinos River Basin, southern Brazil. Braz J Biol 75:S98–S104CrossRefGoogle Scholar
  14. Bergamaschi B, Rodrigues MT, Silva JVS, Kluge M, Luz RB, Fleck JD, Bianchi E, Silva LB, Spilki FR (2015) Moving beyond classical markers of water quality: detection of enteric viruses and genotoxicity in water of the Sinos River. Braz J Biol 75(S2):S63–S67CrossRefGoogle Scholar
  15. Biagini FR, David JAO, Fontanetti CS (2009) The use of histological, histochemical and ultramorphological techniques to detect gill alteration in Oreochromis niloticus reared in treated polluted waters. Micron 40(8):839–844. CrossRefGoogle Scholar
  16. 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):S68–S74CrossRefGoogle Scholar
  17. Bianchi E, Lessing G, Brina KR, Angeli L, Andriguetti NB, Peruzzo JRS, Nascimento CA, Spilki FR, Ziulkoski AL, Silva LB (2017) Monitoring the genotoxic and cytotoxic potential and the presence of pesticides and hydrocarbons in water of the Sinos River basin, southern Brazil. Arch Environ Contam Toxicol 72(3):321–334. CrossRefGoogle Scholar
  18. Bieger L, Carvalho ABP, Strieder MN, Maltchik L, Stenert C (2010) Are the streams of the Sinos River basin of good quality? Aquatic macroinvertebrates may answer the question. Braz J Biol 70(4):1207–1215. CrossRefGoogle Scholar
  19. Bizzotto PM, Godinho AL, Vono V, Kynard B, Godinho HP (2009) Influence of seasonal, diel, lunar, and other environmental factors on upstream fish passage in the Igarapava Fish Ladder, Brazil. Ecol Freshw Fish 18(3):461–472Google Scholar
  20. Blume KK, Macedo JC, Meneguzzi A, Silva LB, Quevedo DM, Rodrigues MAR (2010) Water quality assessment of the Sinos River, Southern Brazil. Braz J Biol 70(4):1185–1193. CrossRefGoogle Scholar
  21. Bohonak AJ, van der Linde K (2004) RMA: software for reduced major axis regression, Java version. Accessed 14 August 2017
  22. Bolger T, Connolly PL (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34(2):171–182. CrossRefGoogle Scholar
  23. Bolognesi C, Hayashi M (2011) Micronucleus assay in aquatic animals. Mutagenesis 26(1):205–213. CrossRefGoogle Scholar
  24. Bonnineau C, Moeller A, Barata C, Bonet B, Proia L, Sans-Piché F, Schmitt-Jansen M, Guasch H, Segner H (2012) Advances in the multibiomarker approach for risk assessment in aquatic ecosystems. In Emerging and priority pollutants in rivers (pp 147–179). Springer Berlin HeidelbergGoogle Scholar
  25. Bosi G, Arrighi S, Di Giancamillo A, Domeneghini C (2005) Histochemistry of glycoconjugates in mucous cells of Salmo trutta uninfected and naturally parasitized with intestinal helminths. Dis Aquat Org 64(1):45–51. CrossRefGoogle Scholar
  26. Brasil. National Environment Council – CONAMA (2005) Resolução CONAMA 357, de 2005. Accessed 14 July 2016
  27. Breseghelo L, Cardoso MP, Costa MF, Bezerra JC, Yamada ÁT (2004) Efeitos do fluoreto de sódio no epitélio da brânquia do peixe Guaru (Poecilia vivipara). Braz J Vet Res Anim Sci 41:274–280CrossRefGoogle Scholar
  28. Britski HA, Sato Y, Rosa ABS (1988) Manual de identificação de peixes da região de Três Marias, com chave e identificação para os peixes da bacia do rio São Francisco. Brasília: Ed. Ministério da Irrigação –CODEVASF, 3 ed., 115pGoogle Scholar
  29. Brunelli E, Mauceri A, Maisano M, Bernabò I, Giannetto A, De Domenico E, Corapi B, Tripepi S, Fasulo S (2011) Ultrastructural and immunohistochemical investigation on the gills of the teleos, Thalassoma pavo L., exposed to cadmium. Acta Histochem 113(2):201–213. CrossRefGoogle Scholar
  30. Bueno-Krawczyk ACD, Guiloski IC, Piancini LDS, Azevedo JC, Ramsdorf WA, Ide AH, Guimarães ATB, Cestari MM, Silva de Assis HC (2015) Multibiomarker in fish to evaluate a river used to water public supply. Chemosphere 135:257–264. CrossRefGoogle Scholar
  31. Bühler D, Marinowic DR, Rodrigues MAS, Silva LB (2012) Evaluation of genotoxicity and cytotoxicity of treated tannery wastewater in Southern Brazil. Int J Environ Technol Manag 15(2):114–123. CrossRefGoogle Scholar
  32. Caetano DLF, Oliveira EF, Zawadzki CH (2016) Fish species indicators of environmental quality of Neotropical streams in Southern Brazil, upper Paraná river basin. Acta Ichthyol Piscat 46(2):87–96. CrossRefGoogle Scholar
  33. Callegari-Jacques SM (2003) Bioestatística: princípios e aplicações. Artmed, Porto Alegre 255 p Google Scholar
  34. Camargo MP, Martinez CBR (2007) Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotrop Ichthyol 5(3):327–336. CrossRefGoogle Scholar
  35. Carrasco KR, Tilbury KL, Myers MS (1990) Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Can J Fish Aquat Sci 47(11):2123–2136. CrossRefGoogle Scholar
  36. Cassanegro MBB, Droste A (2017) Assessing the spatial pattern of a river water quality in southern Brazil by multivariate analysis of biological and chemical indicators. Braz J Biol 77(1):118–126. CrossRefGoogle Scholar
  37. Cengiz EI, Ünlü E (2002) Histopathological changes in the gills of mosquitofish, Gambusia affinis exposed to endosulfan. Bull Environ Contam Toxicol 68(2):290–296Google Scholar
  38. Cerqueira CC, Fernandes MN (2002) Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish, Prochilodus scrofa. Ecotoxicol Environ Safe 52(2):83–91. CrossRefGoogle Scholar
  39. Colin N, Porte N, 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 540:307–323. CrossRefGoogle Scholar
  40. Comitesinos – Comitê de Gerenciamento da Bacia Hidrográfica do Rio dos Sinos (2009) Accessed 29 June 2016
  41. Costa GM, Benvenuti T, Rubio MAK, Rodrigues MAS, Droste A (2014) Monitoramento químico e do potencial genotóxico para o diagnóstico da qualidade de corpos hídricos. Rev Bras Ciên Amb 32:65–74Google Scholar
  42. Costa PF, Schulz UH (2010) The fish community as an indicator of biotic integrity of the streams in the Sinos River basin. Braz J Biol 70(4 suppl):1195–1205. CrossRefGoogle Scholar
  43. Costa SC, Hartz SM (2009) Evaluation of trace metals (cadmium, chromium, copper and zinc) in tissues of a commercially important fish (Leporinus obtusidens) from Guaíba Lake, Southern Brazil. Braz Arch Biol Technol 52(1):241–250. CrossRefGoogle Scholar
  44. Covello JM, Bird S, Morrison RN, Battaglene SC, Secombes CJ, Nowak BF (2009) Cloning and expression analysis of three striped trumpeter (Latris lineata) pro-inflammatory cytokines, TNF-α, IL-1β and IL-8, in response to infection by the ectoparasitic, Chondracanthus goldsmidi. Fish Shellfish Immun 26(5):773–786. CrossRefGoogle Scholar
  45. Cruz AL, Prado TM, Maciel LAS, Couto RD (2015) Environmental effects on the gills and blood of Oreochromis niloticus exposed to rivers of Bahia, Brazil. Ecotox Environ Safe 111:23–31. CrossRefGoogle Scholar
  46. Dalzochio T, Rodrigues GZP, Petry IE, Gehlen G, Silva LB (2016) The use of biomarkers to assess the health of aquatic ecosystems in Brazil: a review. Int Aquat Res 8(4):283–298. CrossRefGoogle Scholar
  47. Depledge MH, Aagaard A, Györkös P (1995) Assessment of trace metal toxicity using molecular, physiological and behavioural biomarkers. Mar Poll Bull 31(1):19–27. CrossRefGoogle Scholar
  48. Dezfuli BS, Pironi F, Campisi M, Shinn AP, Giari L (2010) The response of intestinal mucous cells to the presence of enteric helminths: their distribution, histochemistry and fine structure. J Fish Dis 33(6):481–488. CrossRefGoogle Scholar
  49. Fasulo S, Mauceri A, Maisano M, Giannetto A, Parrino V, Gennuso F, D’Agata A (2010) Immunohistochemical and molecular biomarkers in Coris julis exposed to environmental contaminants. Ecotox Environ Safe 73(5):873–882. CrossRefGoogle Scholar
  50. Figueiredo JAS, Drumm E, Rodrigues MAS, Spilki FR (2010) The Rio dos Sinos watershed: an economic and social space and its interface with environmental status. Braz J Biol 70(S4):1131–1136. CrossRefGoogle Scholar
  51. Foy CD, Chancy RL, White MC (1978) The physiology of metal toxicity in plants. Ann Rev Plant Phys 29(1):511–566. CrossRefGoogle Scholar
  52. Gammons CH, Slotton DG, Gerbrandt B, Weight W, Young CA, McNearly RL, Cámac E, Calderón R, Tapia H (2006) Mercury concentration on fish, river water, and sediment in the Rio Ramis-Lake Titicaca watershed, Peru. Sci Total Environ 368(2-3):637–648. CrossRefGoogle Scholar
  53. Giulio RT, Washburn PC, Wenning RJ (1989) Biochemical responses in aquatic animals—a review of determinants of oxidative stress. Environ Toxicol Chem 8(12):1103–1123. CrossRefGoogle Scholar
  54. Gravato C, Santos MA (2002) β-Naphthoflavone liver EROD and erythrocytic nuclear abnormality induction in juvenile Dicentrarchus labrax. Ecotoxicol Environ Safe 52(1):69–74. CrossRefGoogle Scholar
  55. Grisolia CK, Rivero CLG, Starling FLRM, Silva ICR, Barbosa AC, Dorea JG (2009) Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genet Mol Biol 32(1):138–143. CrossRefGoogle Scholar
  56. Hatje V, Bidone ED, Maddock JL (1998) Estimation of the natural and anthropogenic components of heavy metal fluxes in fresh water Sinos River, Rio Grande do Sul State, South Brazil. Environ Technol 19(5):483–487. CrossRefGoogle Scholar
  57. Henry F, Amara R, Courcot L, Lacouture D, Bertho ML (2004) Heavy metals in four fish species from the French coast of the Eastern English Channel and Southern Bight of the North Sea. Environ Int 30(5):675–683. CrossRefGoogle Scholar
  58. Instituto Brasileiro de Geografia e Estatística – IBGE. Indicadores de Desenvolvimento Sustentável – Brasil (2010) Accessed 20 December 2016
  59. Jager T, Barsi A, Hamda NT, Martin BT, Zimmer EI, Ducrot V (2014) Dynamic energy budgets in population ecotoxicology: applications and outlook. Ecol Model 280:140–147. CrossRefGoogle Scholar
  60. Jarić I, Višnjić-Jeftić Ž, Cvijanović G, Gačić Z, Jovanović L, Skorić S, Lenhardt M (2011) Determination of differential heavy metal and trace element accumulation in liver, gills, intestine and muscle of sterlet (Acipenser ruthenus) from the Danube River in Serbia by ICP-OES. Microchem J 98(1):77–81. CrossRefGoogle Scholar
  61. Javed M, Ahmad I, Usmani N, Ahmad M (2016) Studies on biomarkers of oxidative stress and associated genotoxicity and histopathology in Channa punctatus from heavy metal polluted canal. Chemosphere 151:210–219. CrossRefGoogle Scholar
  62. Jesus IS, Cestari MM, Bezerra MA, Affonso PRAM (2016) Genotoxicity effects in freshwater fish from a Brazilian impacted river. Bull Environ Contam Toxicol 96(4):490–495. CrossRefGoogle Scholar
  63. Jiao W, Chen W, Chang AC, Page AL (2012) Environmental risks of trace elements associated with long-term phosphate fertilizers applications: a review. Environ Poll 168:44–53. CrossRefGoogle Scholar
  64. Kieling-Rubio MA, Benvenuti T, Costa GM, Petry CT, Rodrigues MAS, Schmitt JL, Droste A (2015) Integrated environmental assessment of streams in the Sinos River basin in the state of Rio Grande do Sul, Brazil. Braz J Biol 75(2):S105–S113CrossRefGoogle Scholar
  65. Konzen GB, Figueiredo JAS, Quevedo DM (2015) History of water quality parameters—a study on the Sinos River/Brazil. Braz J Biol 75(2):S1–S10CrossRefGoogle Scholar
  66. Kosanovic M, Hasan MY, Subramanian D, Al Ahbabi AAF, Al Kathiri OAA, Aleassa EMAA, Adem A (2007) Influence of urbanization of the western coast of the United Arab Emirates on trace metal content in muscle and liver of wild Red-spot emperor (Lethrinus lentjan). Food Chem Toxicol 45(11):2261–2266Google Scholar
  67. Lampert VR, Azevedo MA, Fialho CB (2004) Reproductive biology of Bryconamericus iheringii (Ostariophysi: Characidae) from rio Vacacaí, RS, Brazil. Neotrop Ichthyol 2(4):209–215. CrossRefGoogle Scholar
  68. Ledy K, Giambérini L, Pihan JC (2003) Mucous cell responses in gill and skin of brown trout Salmo trutta fario in acidic, aluminium-containing stream water. Dis Aquat Org 56(3):235–240. CrossRefGoogle Scholar
  69. Lemos CT, Iranço FA, Oliveira NCD, Souza GD, Fachel JMG (2008) Biomonitoring of genotoxicity using micronuclei assay in native population of Astyanax jacuhiensis (Characiformes: Characidae) at sites under petrochemical influence. Sci Total Environ 406(1-2):337–343. CrossRefGoogle Scholar
  70. Linde-Arias AR, Inácio AF, Alburquerque C, Freire MM, Moreira JC (2008) Biomarkers in an invasive fish species, Oreochromis niloticus, to assess the effects of pollution in a highly degraded Brazilian river. Sci Total Environ 399(1-3):186–192. CrossRefGoogle Scholar
  71. Loro VL, Murussi C, Menezes C, Leitemperger J, Severo E, Guerra L, Costa M, Perazzo GX, Zanella R (2015) Spatial and temporal biomarkers responses of Astyanax jacuhiensis (Cope, 1894) (Characiformes: Characidae) from the middle Rio Uruguai, Brazil. Neotropl Ichthyol 13(3):569–578. CrossRefGoogle Scholar
  72. Maceda-Veiga A, Green AJ, Poulin R, Lagrue C (2016) Body condition peaks at intermediate parasite loads in the common bully Gobiomorphus cotidianus. PLoS One 11(12):e0168992. CrossRefGoogle Scholar
  73. Maceda-Veiga A, Green AJ, Sostoa A (2014) Scaled body-mass index shows how habitat quality influences the condition of four fish taxa in north-eastern Spain and provides a novel indicator of ecosystem health. Freshw Biol 59(6):1145–1160. CrossRefGoogle Scholar
  74. Mallat J (1985) Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 42(4):630–648. CrossRefGoogle Scholar
  75. Marcato ACC, Yabuki AT, Fontanetti CS (2014) Nickel exposure promotes osmoregulatory disturbances in Oreochromis niloticus gills: histopathological and energy dispersive spectrometry analysis. Environ Sci Poll Res Int 21(22):13095–13102. CrossRefGoogle Scholar
  76. Monroy M, Maceda-Veiga A, Sostoa A (2014) Metal concentration in water, sediment and four fish species from Lake Titicaca reveals a large-scale environmental concern. Sci Total Environ 487:233–244. CrossRefGoogle Scholar
  77. Monteiro SM, Rocha E, Mancera JM, Fontaínhas-Fernandes A, Sousa M (2009) A stereological study of copper toxicity in gills of Oreochromis niloticus. Ecotoxicol Environ Safe 72(1):213–223. CrossRefGoogle Scholar
  78. Mozsár BA, Boros G, Sály P, Antal L, Nagy SA (2015) Relationship between Fulton’s condition factor and proximate body composition in three freshwater fish species. Appl Ichthyol 31(2):315–320. CrossRefGoogle Scholar
  79. Nascimento CA, Staggemeier R, Bianchi E, Rodrigues MT, Fabres R, Soliman MC, Bortoluzzi M, Luz RB, Heinzelmann LS, Santos EL, Fleck JD, Spilki FR (2015) Monitoring of metals, organic compounds and coliforms in water catchment points from the Sinos River basin. Braz J Biol 75(2):S50–S56CrossRefGoogle Scholar
  80. Nunes EA, Lemos CL, Gavronski L, Moreira TN, Oliveira NCD, Silva J (2011) Genotoxic assessment on river water using different biological systems. Chemosphere 84(1):47–53. CrossRefGoogle Scholar
  81. Ohe T, Watanabe T, Wakabayashi K (2004) Mutagens in surface waters: a review. Mutat Res 567(2–3):109–149. CrossRefGoogle Scholar
  82. Oliveira MTG, Rolim SBA, Mello-Farias PC, Meneguzzi A, Lutckmeier C (2008) Industrial pollution of environmental compartments in the Sinos River Valley, RS, Brazil: geochemical-biogeochemical characterization and remote sensing. Water Air Soil Poll 192(1-4):183–198. CrossRefGoogle Scholar
  83. Pacheco M, Santos MA (1998) Induction of liver EROD and erythrocytic nuclear abnormalities by cyclophosphamide and PAHs in Anguilla anguilla L. Ecotox Environ Safe 40(1-2):71–76. CrossRefGoogle Scholar
  84. Paulino MG, Benze TP, Sadauskas-Henrique H, Sakuragui MM, Fernandes JB, Fernandes MN (2014) The impact of organochlorines and metals on wild fish living in a tropical hydroelectric reservoir: bioaccumulation and histopathological biomarkers. Sci Total Environ 497:293–306CrossRefGoogle Scholar
  85. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118(12):1883–1891. CrossRefGoogle Scholar
  86. Pedde V, Figueiredo JAS, Nunes MF, Prodanov CC (2015) Environment and society: the Sinos River Basin and public policies. Braz J Biol 75(2):S128–S136CrossRefGoogle Scholar
  87. Perry SF, Laurent P (1993) Environmental effects on fish gill structure and function. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 231–264. CrossRefGoogle Scholar
  88. Poleksic V, Mitrovic-Tutundzic V (1994) Fish gills as a monitor of sublethal and chronic effects of pollution. In: Muller R, Lloyd R (eds) Sublethal and chronic effects of pollutants on freshwater fish. Fishing News Books, Oxford, pp p339–p352Google Scholar
  89. Porto JIR, Araujo CSO, Feldberg E (2005) Mutagenic effects of mercury pollution as revealed by micronucleus test on three Amazonian fish species. Environ Res 97(3):287–292. CrossRefGoogle Scholar
  90. Procópio MS, Ribeiro HJ, Pereira LA, Lopes GAO, Castro ACS, Rizzo E, Sato Y, Russo RC, Junior JDC (2014) Sex-response differences of immunological and histopathological biomarkers in gill of Prochilodus argenteus from a polluted river in southeast Brazil. Fish Shellfish Immun 39(1):108–117. CrossRefGoogle Scholar
  91. Rechenmacher C, Siebel AM, Goldoni A, Klauck CR, Sartori T, Rodrigues MT, Rodrigues MAS, Gehlen G, Ardenghi PG, Silva LB (2010) A multibiomarker approach to assess the impact of pollution on Sinos River, southern Brazil. Braz J Biol 70(4):1223–1230. CrossRefGoogle Scholar
  92. Ribeiro DL, Barcelos GRM, d’Arce LPG (2014) Genotoxic effects of water from São Francisco River, Brazil, in Astyanax paranae. Bull Environ Contam Toxicol 93(3):274–279. CrossRefGoogle Scholar
  93. Saboaia-Moraes SMT, Hernandez-Blazquez FJ, Mota DL, Bittencourt AM (1996) Mucous cell types in the branchial epithelium of the euryhaline fish Poecilia vivipara. J Fish Biol 49(3):545–548. CrossRefGoogle Scholar
  94. Salvagni J, Ternus RZ, Fuentefria AM (2011) Assessment of the genotoxic impact of pesticides on farming communities in the countryside of Santa Catarina State, Brazil. Genet Mol Biol 34(1):122–126. CrossRefGoogle Scholar
  95. Sanchez W, Piccini B, Ditche JM, Porcher JM (2008) Assessment of seasonal variability of biomarkers in three-spined stickleback (Gasterosteus aculeatus L.) from a low contaminated stream: implication for environmental biomonitoring. Environ Int 34(6):791–798. CrossRefGoogle Scholar
  96. Scalon MCS, Rechenmacher C, Siebel AM, Kayser ML, Rodrigues MT, Maluf SW, Rodrigues MT, Maluf SW, Rodrigues MAS, Silva LB (2010) Evaluation of Sinos River water genotoxicity using the comet assay in fish. Braz J Biol 70(4):1217–1222. CrossRefGoogle Scholar
  97. Seriani R, Abessa DMS, Moreira LB, Cabrera JPG, Sanches JQ, Silva CLS, Amorin FA, Rivero DHRF, Fitorra LS, Carvalho-Oliveira R, Macchione M, Ranzani-Paiva MJT (2015) In vitro mucus transportability, cytogenotoxicity, and hematological changes as non-destructive physiological biomarkers in fish chronically exposed to metals. Ecotox Environ Safe 112:162–168. CrossRefGoogle Scholar
  98. Shinn C, Dauba F, Grenouillet G, Guenard G, Lek S (2009) Temporal variation of heavy metal contamination in fish of the river lot in southern France. Ecotoxl Environ Safe 72(7):1957–1965. CrossRefGoogle Scholar
  99. Souza IC, Duarte ID, Pimentel NQ, Rocha LD, Morozesk M, Bonomo MM, Azevedo VC, Pereira CDS, Monferrán MV, Milanez CRD, Matsumoto ST, Wunderlin DA Fernandes MN (2013) Matching metal pollution with bioavailability, bioaccumulation and biomarkers response in fish (Centropomus parallelus) resident in neotropical estuaries. Environ Poll 180:136–144. CrossRefGoogle Scholar
  100. Steffens C, Klauck CR, Benvenuti T, Silva LB, Rodrigues MAS (2015) Water quality assessment of the Sinos River-RS, Brazil. Braz J Biol 75(4):62–67. CrossRefGoogle Scholar
  101. Stevenson RD, Woods WA Jr (2006) Condition indices for conservation: new uses for evolving tools. Integr Comp Biol 46(6):1169–1190. CrossRefGoogle Scholar
  102. Tao S, Wen Y, Long A, Dawson R, Cao J, Xu F (2001) Simulation of acid-base condition and copper speciation in fish gill microenvironment. Comput Chem 25(3):215–222. CrossRefGoogle Scholar
  103. Terra FB, Araújo FG, Calza CF, Lopes RT, Teixeira TP (2008b) Heavy metal in tissues of three fish species from different trophic levels in a tropical Brazilian River. Water Air Soil Poll 187:275–284CrossRefGoogle Scholar
  104. Terra NR, Feiden IR, Fachel JMG, Lemos CT, Nunes EA (2008a) Ecotoxicological evaluation of sediment and water samples from Sinos River, Rio Grande do Sul, Brazil, using Daphnia magna and V79 cells. Acta Limnol Bras 20(1):63–72Google Scholar
  105. Theodorakis CW, Swartz CD, Rogers WJ, Bickham JW, Donnelly KC, Adams SM (2000) Relationship between genotoxicity, mutagenicity, and fish community structure in a contaminated stream. J Aquat Ecosyst Stress Recovery 7(2):131–143. CrossRefGoogle Scholar
  106. Trintinaglia L, Bianchi E, Silva LB, Nascimento CA, Spilki FR, Ziulkoski AL (2015) Cytotoxicity assays as tools to assess water quality in the Sinos River basin. Braz J Biol 75(2):S75–S80CrossRefGoogle Scholar
  107. Udroiu I (2006) The micronucleus test in piscine erythrocytes. Aquat Toxicol 79(2):201–204. CrossRefGoogle Scholar
  108. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13(2):57–149. CrossRefGoogle Scholar
  109. 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 Total Environ 542(Pt A):44–56. CrossRefGoogle Scholar
  110. Yilmaz AB (2003) Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environ Res 92(3):277–281. CrossRefGoogle Scholar
  111. Wang WX, Rainbow PS (2008) Comparative approaches to understand metal bioaccumulation in aquatic animals. Comp Biochem Physiol C 148:315–323Google Scholar
  112. Weather Underground (2015)>. Accessed 26 April 2016
  113. Weber P, Behr ER, Knorr CL, Vendruscolo DS, Flores EMM, Dressler VL, Baldisserotto B (2013) Metals in the water, sediment, and tissues of two fish species from different trophic levels in a subtropical Brazilian river. Microchem J 106:61–66. CrossRefGoogle Scholar
  114. Wendelaar-Bonga SE (1997) The stress response in fish. Physiol Rev 77(3):591–625. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Thaís Dalzochio
    • 1
  • Gabriela Zimmermann Prado Rodrigues
    • 1
  • Leonardo Airton Ressel Simões
    • 2
  • Mateus Santos de Souza
    • 2
  • Ismael Evandro Petry
    • 2
  • Natália Bordin Andriguetti
    • 3
  • Gláucia Joselaine Herbert Silva
    • 4
  • Luciano Basso da Silva
    • 1
  • Günther Gehlen
    • 1
  1. 1.Programa de Pós-Graduação em Qualidade AmbientalUniversidade FeevaleNovo HamburgoBrazil
  2. 2.Curso de Ciências BiológicasUniversidade FeevaleNovo HamburgoBrazil
  3. 3.Programa de Pós-graduação em Análises ToxicológicasUniversidade FeevaleNovo HamburgoBrazil
  4. 4.Instituto Federal de Educação, Ciência e Tecnologia do Rio Grande do SulFelizBrazil

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