Is There Detectable Long-term Depletion of Genetic Variation in Freshwater Fish Species Affected by an Oil Spill?

  • André O. Agostinis
  • Giorgi Dal Pont
  • Aline Horodesky
  • Marcio R. PieEmail author
  • Antonio Ostrensky


Oil spills might lead to severe environmental impacts to the affected fauna, disrupting local food webs, and causing mass mortality in many species. However, little is known about long-term impacts of oil spills, or even if such impacts can be detectable after several generations. In this study, we investigate the genetic variability of three freshwater species—Mimagoniates microlepis (Characiformes: Characidae), Scleromystax barbatus (Siluriformes: Callichthyidae), and Phalloceros harpagos (Cyprinodontiformes: Poeciliidae)—in rivers that were affected by a large oil spill in the state of Paraná, southern Brazil, on February of 2001. Samples were obtained from nine different locations, such that rivers that were directly affected by the oil spill could be compared with similar rivers in the same region that were unaffected. A fragment of the cytochrome C oxidase subunit I mitochondrial gene was sequenced from each specimen, and the level of genetic variability was assessed. Based on estimates of haplotype and nucleotide diversity, no impact of the oil spill could be detected in impacted rivers. These results suggest that fish populations in the region showed resilience to the pollutant, such that immigration from other locations was able to reestablish levels of genetic variability comparable to those of unimpacted rivers.


Genetic variability Mimagoniates microlepis Scleromystax barbatus Phalloceros harpagos Environmental impact 



The authors thank the Brazilian National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq) for providing a productivity in research grant to Antonio Ostrensky. We also thank the Brazilian Federal Agency for Support and Evaluation of Graduate Education (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior —CAPES) for providing PhD grant to Giorgi Dal Pont and Aline Horodesky.

Compliance with Ethical Standards

Conflict of Interest

This study was funded by Petrobras (grant). However, the source of type of funding was categorized explicitly as a research project, and there was no influence or oversight from the funders on the analyses, results, and writing of this manuscript.


  1. Albarello, L.C. (2012). O vazamento do oleoduto OLAPA (Morretes, Paraná): Avaliação ambiental e reconstituição do óleo, da Serra do Mar ao complexo estuarino de Paranaguá. Pós-Graduação em Geociência, Universidade Federal do Rio Grande do Sul, 188 pp. Avaliable at:
  2. Barber, W. E., McDonald, L. L., Erickson, W. P., & Vallarino, M. (1995). Effect of the Exxon Valdez oil spill on intertidal fish: a field study. Transactions of the American Fisheries Society, 124, 461–476.CrossRefGoogle Scholar
  3. Barron, M. G., Podrabsky, T., Ogle, S., & Ricker, R. W. (1999). Are aromatic hydrocarbons the primary determinant of petroleum toxicity to aquatic organisms? Aquatic Toxicology, 46, 253–268.CrossRefGoogle Scholar
  4. Bickham, J. W., Sandhu, S., Hebert, P. D. N., Chikhi, L. & Athwal R. (2000). Effects of chemicals contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutation Research/ Reviews in Mutation Research, 463(1): 33–51.Google Scholar
  5. Boeger, W.A., Guimarães, A.T.B., Romão, S., Ostrensky, A., ZAmberlan, E. & Falkiewicz, F.H. 2003. Histopatology as an approach to evaluated the effect of an oil spill on fishes of Arroio Saldanha and Rio Iguaçu (Brazil), International oil spill conference, Amer Petroleum Inst, Washington, USA.Google Scholar
  6. Bolognesi, C., Perrone, E., Roggieri, P., & Sciutto, A. (2006). Bioindicators in monitoring long term genotoxic impact of oil spill: haven case study. Marine Environmental Research, 62(Supplement 1), S287–S291.CrossRefGoogle Scholar
  7. Carls, M. G., Rice, S. D., & Hose, J. E. (1999). Sensitivity of fish embryos to weathered crude oil: part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval pacific herring (Clupea pallasi). Environmental Toxicology and Chemistry, 18, 481–493.CrossRefGoogle Scholar
  8. Collier, T.K., Krone, C.A., Krahn, M.M., Stein, J.E., Chan, S.L. & Varanasi, U. 1996. Petroleum exposure and associated biochemical effects in subtidal fish after the Exxon Valdez oil spill American Fisheries Society Symposium, pp. 671–683. Avaliable on.Google Scholar
  9. Cronin, M. A., & Bickham, J. W. (1998). A population genetic analysis of the potential for a crude oil spill to induce heritable mutations and impact natural populations. Ecotoxicology, 7, 259–278.CrossRefGoogle Scholar
  10. Eisler, R. (1987). Polycyclic aromatic hydrocarbon hazards to fish, wildlife, and invertebrates: a synoptic review. US fish and wildlife service biological report, 85, 81.Google Scholar
  11. Etkin, D.S. 2004 Modeling oil spill response and damage costs Proceedings of the Fifth Biennial Freshwater Spills Symposium, p. 16. Avaliable at:
  12. Faria, B.M.D., Timmerman, M.C., Platte, E.B. & Rosário, M.D. (2005). Environmental effects in a subtropical brazilian river after an oil spill International Oil Spill Conference Proceedings, pp. 701–702. Avaliable at:
  13. Gabardo, I.T., Meniconi, M.F., Faria, B.M., Silva, T.A., Cavalcanti, T.R., Silva, G.C., Gallotta, F.D., N., A.S., Paes, J.E., Bentz, C.M., Lima, S.O.F., Rosário, M.D., Soriano, A.U., Baessa, M.P.M., Mendes, L.G., Dirceu C, Silveira, J., Bilhalva, M.M., Politano, A.T., Freitas, L.R.D., Parkinson, R., Lima, J.A.M., Guimarães, P.P., Medeiros, J. & Santos, A.F. 2011. Lessons learned on oil spill environment impact assessment: 10 years of petrobras experience review. International Oil Spill Conference Proceedings, p. abs426. Avaliable at:
  14. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
  15. Harvey, R. G. (1991). Polycyclic aromatic hydrocarbons: chemistry and carcinogenicity (p. 396). Cambridge: CAmbridge Universaty Press.Google Scholar
  16. Horodesky, A., Abilhoa, V., Zeni, T. D. O., Montanhini Neto, R., Castilho-Westphal, G. G., & Ostrensky, A. (2015). Ecological analysis of the ichthyofaunal community ten years after a diesel oil spill at Serra do Mar, Paraná state, Brazil. Global Ecology and Conservation, 4, 311–320.CrossRefGoogle Scholar
  17. Hose, J. E., McGurk, M. D., Marty, G. D., Hinton, D. E., Brown, E. D., & Baker, T. T. (1996). Sublethal effects of the (Exxon Valdez) oil spill on herring embryos and larvae: morphological, cytogenetic, and histopathological assessments, 1989–1991. Canadian Journal of Fisheries and Aquatic Sciences, 53, 2355–2365.Google Scholar
  18. Incardona, J. P., Collier, T. K., & Scholz, N. L. (2004). Defects in cardiac function precede morphological abnormalities in fish embryos exposed to polycyclic aromatic hydrocarbons. Toxicology and Applied Pharmacology, 196, 191–205.Google Scholar
  19. Incardona, J. P., Vines, C. A., Linbo, T. L., Myers, M. S., Sloan, C. A., Anulacion, B. F., Boyd, D., Collier, T. K., Morgan, S., Cherr, G. N., & Scholz, N. L. (2012). Potent phototoxicity of marine bunker oil to translucent herring embryos after prolonged weathering. PloS One, 7, 30116.CrossRefGoogle Scholar
  20. Katsumiti, A., França, P. P., Costa, G. P. S., Zandoná, E. M., Benincá, C., Assis, H. C. S. D., Cestari, M. M., Maschchio, J., Randi, M. A. F., Silva, C. A., Rochecheche, H., & Ribebeiro, C. A. O. (2013). Evaluation five years after a refinary oil spill in freshwater wetland—Paraná State, Southern of Brazil. Ecotoxicology and Environmental Contamination, 8, 77–87.CrossRefGoogle Scholar
  21. Lanctot, R., Goatcher, B., Kim, S., Talbot, S., Pierson, B., Daniel, E., & Zwiefelhofer, D. (1999). Harlequin duck recovery from the Exxon Valdez oil spill: a population genetics perspective. The Auk, 116, 781–791.CrossRefGoogle Scholar
  22. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., & Higgins, D. G. (2007). Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947–2948.CrossRefGoogle Scholar
  23. Librado, P. & Rozas, J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.Google Scholar
  24. Miller, G. D., Seeb, J. E., Bue, B. G., & Sharr, S. (1994). Saltwater exposure at fertilization induces ploidy alterations. Including mosaicism, in salmonid. Canadian Journal of Fisheries and Aquatic Sciences, 51, 42–49.CrossRefGoogle Scholar
  25. Ostrensky, A., Chaves, P.T.C., Duboc, L.F., Guimarães, A.T.B., Cruz, S.R.Z., Wegbecher, F.X., Pilchowski, R.W., Teixeira, U.A. & Belz, C.E. (2001). Monitoramento ictiofaunístico pós-derramamento de óleo nos Rios Bariguí e Iguaçu, 2° Seminário do Rio Iguaçu, Araucária, Paraná, Brasil, pp. 32–52.Google Scholar
  26. Ostrensky, A., Neto, R. M., Castilho-Westphal, G. G., Zeni, T. O., Abilhoa, V., & Horodesky, A. (2015). Population structure of fish from the Serra do Mar, Paraná, Brazil: a comparative analysis of environments affected and by oil spills and unaffected areas. Journal of Ecology and The Natural Environment, 1, 54–62.Google Scholar
  27. Paradis, E. (2010). pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419–420.Google Scholar
  28. Peterson, C. H., Rice, S. D., Short, J. W., Esler, D., Bodkin, J. L., Ballachey, B. E., & Irons, D. B. (2003). Long-term ecosystem response to the Exxon Valdez oil spill. Science, 302, 2082–2086.CrossRefGoogle Scholar
  29. R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 19 January 2017.
  30. Srogi, K. (2007). Monitoring of environmental exposure to polycyclic aromatic hydrocarbons: a review. Environmental Chemistry Letters, 5, 169–195.CrossRefGoogle Scholar
  31. Staden, R., Beal, K. F. & Bonfield, J. K. (1998). The staden package. Computer methods in molecular biology, bioinformatics methods and protocols. In S. Misener & S. A. Krawetz (Eds), The Humana Press Inc., Totowa, NJ 07512, 132, 15–130.Google Scholar
  32. Teal, J. M., & Howarth, R. W. (1984). Oil spill studies: a review of ecological effects. Environmental Management, 8, 27–43.CrossRefGoogle Scholar
  33. Vanzella, T. P., Martinez, C. B. R., & Cólus, I. M. S. (2007). Genotoxic and mutagenic effects of diesel oil water soluble fraction on a neotropical fish species. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 631, 36–43.CrossRefGoogle Scholar
  34. Wickham, H. (2007). Reshaping data with the reshape package. Journal of Statistical Software, 21, 20.CrossRefGoogle Scholar
  35. Wickham, H. (2011). The split-apply-combine strategy for data analysis. Journal of Statistical Software, 40, 29.Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Grupo Integrado de Aquicultura e Estudos AmbientaisUniversidade Federal do ParanáCuritibaBrazil
  2. 2.Departamento de ZoologiaUniversidade Federal do ParanáCuritibaBrazil
  3. 3.Departamento de ZootecniaUniversidade Federal do ParanáCuritibaBrazil

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