Biochemical effects of pollutant exposure in fish from urban creeks in Greenville, SC (USA)

Abstract

The city of Greenville, SC is a rapidly expanding urban area located on the Reedy River in the upstate of South Carolina. Historical and current point-source pollutants and runoff from impermeable surfaces have resulted in a contaminated river environment, which through previous studies was demonstrated to be reflected in biological effects in fish species in the river. Because it was not known how much smaller tributaries in the urbanized area were contributing to the pollution of the main stem of the Reedy River, we collected fish (bluehead chub (Nocomis leptocephalus), creek chub (Semotilus atromaculatus), bluegill (Lepomis macrochirus), and redbreast sunfish (Lepomis auritus)) from five smaller urban creeks in the Greenville area and measured several biomarkers of exposure in these animals. Enzymatic activities of cytochrome P450-1A (CYP1A) and glutathione S-transferase (GST) were measured, and bile samples were analyzed for fluorescence caused by polynuclear aromatic hydrocarbons (PAHs) and for excreted estrogenic compounds. The results show that some creeks triggered significant biomarker responses in collected fish, while others were relatively clean. In particular, PAHs appear to be prevalent and caused biochemical effects, while estrogenic compounds were not significantly increased in the bile of fish from these urban creeks. A striking observation was the difference in enzyme activities in chub species compared to sunfish species; sunfish had up to five times higher CYP1A activities than chubs, while the chubs had significantly higher GST activity than sunfish. These species differences should be taken into account when they are incorporated in environmental risk assessment and biological effect monitoring programs.

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References

  1. Ankley, G. T., & Agosin, M. (1987). Comparative aspects of hepatic UDP-glucuronosyltransferases and glutathione S-transferases in bluegill and channel catfish. Comparative Biochemistry and Physiology B, 87(4), 671–673.

    CAS  Article  Google Scholar 

  2. Anonymous (2013). Greenville takes lead in banning controversial pavement coating. Greenville News, Section A.

  3. Brammell, B. F., Price, D. J., Birge, W. J., Harmel-Laws, E. M., Hitron, J. A., & Elskus, A. A. (2010). Differential sensitivity of CYP1A to 3,3′,4′,4-tetrachlorobiphenyl and benzo(a)pyrene in two Lepomis species. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 152(1), 42–50.

  4. Chandler, D. M., & Lerner, D. N. (2015). A low cost method to detect polluted surface water outfalls and misconnected drainage. Water and Environment Journal, 29, 202–206.

    CAS  Article  Google Scholar 

  5. Dubé, M. G., MacLatchy, D. L., Hruska, K. A., & Glozier, N. E. (2006). Assessing the responses of creek chub (Semotilus atromaculatus) and pearl dace (Semotilus margarita) to metal mine effluents using in situ artificial streams in Sudbury, Ontario, Canada. Environmental Toxicology and Chemistry, 25(1), 18–28.

    Article  Google Scholar 

  6. Fitzgerald, D. G., Lanno, R. P., & Dixon, D. G. (1999). A comparison of a sentinel species evaluation using creek chub (Semotilus atromaculatus Mitchill) to a fish community evaluation for the initial identification of environmental stressors in small streams. Ecotoxicology, 8, 33–48.

    Article  Google Scholar 

  7. German, D. P., Nagle, B. C., Villeda, J. M., Ruiz, A. M., Thomson, A. W., Contreras, B. S., & Evans, D. H. (2010). Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): effects on gut size and digestive physiology. Physiological and Biochemical Zoology, 83(1), 1–18.

    Article  Google Scholar 

  8. González, J. F., Reimschuessel, R., Shaikh, B., & Kane, A. S. (2009). Kinetics of hepatic phase I and II biotransformation reactions in eight finfish species. Marine Environmental Research, 67(4–5), 183–188.

    Article  Google Scholar 

  9. Henshel, D. S., Sparks, D. W., & Simon, T. P. (2006). Age structure and growth of Semotilus atromaculatus (Mitchill) in PCB-contaminated streams. Journal of Fish Biology, 68, 44–62.

    CAS  Article  Google Scholar 

  10. Jenkins, R. E., & Burkhead, N. M. (1994). The freshwater fishes of Virginia. Bethesda: American Fisheries Society.

    Google Scholar 

  11. Lohner, T. W., Reash, R. J., Willet, V. E., & Rose, L. A. (2001). Assessment of tolerant sunfish populations (Lepomis sp.) inhabiting selenium-laden coal ash effluents: 1. Hematological and population level assessment. Ecotoxicology and Environmental Safety, 50(3), 217–224.

    CAS  Article  Google Scholar 

  12. Mahler, B. J., Van Metre, P. C., & Foreman, W. T. (2014). Concentrations of polycyclic aromatic hydrocarbons (PAHs) and azaarenes in runoff from coal-tar- and asphalt-sealcoated pavement. Environmental Pollution, 188, 81–87.

    CAS  Article  Google Scholar 

  13. Martinovic-Weigelt, D., Minarik, T. A., & Curran, E. M. (2013). Environmental estrogens in an urban aquatic ecosystem: I. Spatial and temporal occurrence of estrogenic activity in effluent-dominated systems. Environment International, 61, 127–137.

    CAS  Article  Google Scholar 

  14. Meador, M. R., & Carlisle, D. M. (2007). Quantifying tolerance indicator values for common stream fish species of the United States. Ecological Indicators, 7, 329–338.

    Article  Google Scholar 

  15. Mierzejewski, J., Haney, D. C., & van den Hurk, P. (2014). Biomarker responses in sunfish and bass from the Saluda river, SC. Ecotoxicology and Environmental Safety, 110, 8–15.

    CAS  Article  Google Scholar 

  16. Oakes, K. D., Sibley, P. K., Martin, J. W., MacLean, D. D., Solomon, K. R., Mabury, S. A., & Van Der Kraak, G. J. (2005). Short-term exposures of fish to perfluorooctane sulfonate: Acute effects on fatty acyl-coa oxidase activity, oxidative stress, and circulating sex steroids. Environmental Toxicology and Chemistry, 24(5), 1172–1181.

    CAS  Article  Google Scholar 

  17. Otter, R. R., Schreiber, E. A., van den Hurk, P., & Klaine, S. J. (2012). Assessment of heavy metal and PAH exposure in largemouth bass (Micropterus salmoides) in the Reedy River watershed, South Carolina, USA: a multi-season assessment of metallothionein and bile fluorescence. Environmental Toxicology and Chemistry, 31(12), 2763–2770.

    CAS  Article  Google Scholar 

  18. Paul, M. J., & Meyer, J. L. (2001). Streams in the urban landscape. Annual Review of Ecology, Evolution, and Systematics, 32, 333–365.

    Article  Google Scholar 

  19. Schlenk, D., Celander, M., Gallagher, E., George, S., James, M., Kullman, S., van den Hurk, P., & Willett, K. (2008). Biotransformation in fishes. In D. Hinton & R. DiGiulio (Eds.), Toxicology of fishes (pp. 153–234). Boca Raton: CRC Press.

    Google Scholar 

  20. Schorr, M. S., & Backer, J. C. (2006). Localized effects of coal mine drainage on fish assemblages in a Cumberland Plateau stream in Tennessee. Journal of Freshwater Ecology, 21, 17–24.

    CAS  Article  Google Scholar 

  21. Schreiber, E. A., Otter, R. R., & van den Hurk, P. (2006). A biomarker approach to measure biological effects of contaminant exposure in largemouth bass from Lake Conestee, SC, USA. Environmental Toxicology and Chemistry, 25, 1829–1835.

    Article  Google Scholar 

  22. Sekabira, K., Origa, H. O., & Basamba, T. A. (2010). Heavy metal assessment and water quality values in urban stream and rain water. International journal of Environmental Science and Technology, 7, 759–770.

    CAS  Article  Google Scholar 

  23. Selbig, W. R., Bannerman, R., & Corsi, S. R. (2013). From streets to streams: assessing the toxicity potential of urban sediment by particle size. Science of the Total Environment, 444, 381–391.

    CAS  Article  Google Scholar 

  24. Siligato, S., & Boehmer, J. (2002). Evaluation of biological integrity of a small urban stream system by investigating longitudinal variability of the fish assemblage. Chemosphere, 47, 777–788.

    CAS  Article  Google Scholar 

  25. Stair, D. M., Tolbert, V. R., & Vaughan, G. L. (1984). Comparison of growth, population-structure, and food of the creek chub Semotilus atromaculatus in undisturbed and surface-mining-disturbed streams in Tennessee. Environmental Pollution Series A, 35, 331–343.

    Article  Google Scholar 

  26. Truman, P. A., & van den Hurk, P. (2010). A biomarker approach examining xenoestrogen exposure in bluegill in the Reedy River watershed, SC, USA. Archives of Environmental Contamination and Toxicology, 58(1), 165–175.

    CAS  Article  Google Scholar 

  27. USDA. (2012). National agricultural statistics service cropland data layer [internet]. Washington (DC): USDA-NASS Available from: http://nassgeodata.gmu.edu/CropScape/.

    Google Scholar 

  28. van den Hurk, P. (2006). Bile fluorescence, heme oxygenase induction, and increased biliverdin excretion by mixtures of environmental toxicants. Aquatic Toxicology, 77, 202–209.

    Article  Google Scholar 

  29. van der Oost, R., Beyer, J., & Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13, 57–149.

    Article  Google Scholar 

  30. Vandepoele, K., De Vos, W., & Taylor, J. S. (2004). Major events in the genome evolution of vertebrates: Paranome age and size differ considerably between ray-finned fishes and land vertebrates. Proceedings of the National Academy of Sciences USA, 101, 1638–1643.

    CAS  Article  Google Scholar 

  31. Wallace, A. M., Croft-White, M. V., & Moryk, J. (2013). Are Toronto’s streams sick? A look at the fish and benthic invertebrate communities in the Toronto region in relation to the urban stream syndrome. Environmental Monitoring and Assessment, 185, 7857–7875.

    Article  Google Scholar 

  32. Walsh, C. J., Roy, A. H., Feminella, J. W., Cottingham, P. D., Groffman, P. M., & Morgan, R. P. (2005). The urban stream syndrome: current knowledge and the search for a cure. Journal of the North American Benthological Society, 24, 706–723.

    Article  Google Scholar 

  33. Witter, A. E., Nguyen, M. H., Baidar, S., & Sak, P. B. (2014). Coal-tar-based sealcoated pavement: a major PAH source to urban stream sediments. Environmental Pollution, 185, 59–68.

    CAS  Article  Google Scholar 

  34. Yang, Y., Van Metre, P. C., Mahler, B. J., Wilson, J. T., Ligouis, B., Razzaque, M. D., Schaeffer, D. J., & Werth, C. J. (2010). Influence of coal-tar sealcoat and other carbonaceous materials on polycyclic aromatic hydrocarbon loading in an urban watershed. Environmental Science and Technology, 44(4), 1217–1223.

    CAS  Article  Google Scholar 

  35. Yang, Y. Y., Toor, G. S., & Williams, C. F. (2015). Pharmaceuticals and organochlorine pesticides in sediments of an urban river in Florida. Journal of Soils and Sediments, 15, 993–1004.

    CAS  Article  Google Scholar 

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Acknowledgements

Assistance with field sampling was provided by Chisom Onyeuku from Furman University. In addition, field work assistance and some of the biomarker analyses were performed with help from Clemson University graduate students Diana Delach and Phenny Mwaanga. This project was partially funded through a grant from the South Carolina Water Resources Center. Furman University students were financially supported by the Furman Advantage Program.

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Correspondence to Dennis C. Haney.

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van den Hurk, P., Haney, D.C. Biochemical effects of pollutant exposure in fish from urban creeks in Greenville, SC (USA). Environ Monit Assess 189, 211 (2017). https://doi.org/10.1007/s10661-017-5918-2

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Keywords

  • Biomarkers
  • Fish
  • Urban creeks
  • PAH