Advertisement

Metal contamination and food web changes alter exposure to upper trophic levels in upper Blackfoot River basin streams, Montana

  • Jack Landers
  • Sean Sullivan
  • Lisa Eby
  • Andrew C. Wilcox
  • Heiko Langner
Primary Research Paper
  • 20 Downloads

Abstract

Reduced invertebrate abundance and diversity are common responses to metals contamination in mining-impacted streams. The resulting changes in community composition may have implications for metals accumulation and transfer through the food web. We investigated how changes in invertebrate community composition (abundance, species richness, and food web complexity) influence metals bioaccumulation and exposure risk to upper trophic levels along a contamination gradient in the upper Blackfoot River Basin, Montana. Invertebrate species richness exhibited the strongest decline with increasing sediment metals concentrations, driven by the loss of metals-sensitive taxa. These changes in invertebrate community composition resulted in a decline in the proportion of invertebrates in the scraper functional feeding group, likely influencing dietary metals exposure to the invertebrate community. Additionally, invertebrates with a strong propensity-to-drift increased with sediment contamination, potentially facilitating metals transfer to fish and higher trophic levels through predation. Using invertebrate exposure values (invertebrate abundance × metals concentrations), we found that moderately contaminated sites in our study area produced both the highest invertebrate exposure values and the highest fish tissue metals concentrations. Considering both changes in invertebrate community composition and metal concentrations is an important step towards understanding and evaluating potential toxic effects to upper trophic levels in mining-impacted streams.

Keywords

Pollution Macroinvertebrate community structure Aquatic communities Acid mine drainage Upper blackfoot mining complex 

Notes

Acknowledgements

This research was funded by the US Environmental Protection Agency and the US Forest Service. We thank Nick Hehemann, Robert Livesay, Doug Brinkerhoff, and Matt Corsi for field data collection and Johnnie Moore for guidance. We also thank Will Clements and anonymous reviewers for comments that greatly improved the manuscript.

Supplementary material

10750_2018_3857_MOESM1_ESM.xlsx (68 kb)
Supplementary material 1 (XLSX 67 kb)
10750_2018_3857_MOESM2_ESM.xlsx (28 kb)
Supplementary material 2 (XLSX 28 kb)
10750_2018_3857_MOESM3_ESM.xlsx (128 kb)
Supplementary material 3 (XLSX 127 kb)
10750_2018_3857_MOESM4_ESM.xlsx (24 kb)
Supplementary material 4 (XLSX 24 kb)

References

  1. Akaike, H., 1973. Information theory as an extension of the maximum likelihood principle In Petrov, B., & F. Csaki (eds), Second international symposium on information theory. Akaemiai Kiado, Budapest: 267–281.Google Scholar
  2. Allan, D. J., 1981. Determinants of diet of brook trout (Salvelinus fontinalis) in a mountain stream. Canadian Journal of Fisheries and Aquatic Sciences 38: 184–192.CrossRefGoogle Scholar
  3. August, E. E., D. M. McKnight, D. C. Hrncir & K. S. Garhart, 2002. Seasonal variability of metals transport through a wetland impacted by mine drainage in the Rocky Mountains. Environmental Science & Technology 36: 3779–3786.CrossRefGoogle Scholar
  4. Axtmann, E. V., D. J. Cain & S. N. Luoma, 1997. Effect of tributary inflows on the distribution of trace metals in fine- grained bed sediments and benthic insects of the Clark Fork River, Montana. Environmental Science and Technology 31: 750–758.CrossRefGoogle Scholar
  5. Beltman, D. J. B., W. H. Clements, J. Lipton & D. Cacela, 1999. Benthic invertebrate metals exposure, accumulation, and community-level effects downstream from a hard-rock mine site. Environmental Toxicology and Chemistry 18: 299–307.CrossRefGoogle Scholar
  6. Bersier, L. F., C. Banašek-Richter & M. F. Cattin, 2002. Quantitative descriptors of food-web matrices. Ecology 83: 2394–2407.CrossRefGoogle Scholar
  7. Besser, J. M., W. G. Brumbaugh, T. W. May, S. E. Church & B. A. Kimball, 2001. Bioavailability of metals in stream food webs and hazards to brook trout (Salvelinus fontinalis) in the upper Animas River watershed, Colorado. Archives of Environmental Contamination and Toxicology 40: 48–59.CrossRefGoogle Scholar
  8. Bureau of Land Management, 2014. Abandoned Mine Land Inventory Study for BLM-Managed Lands in California, Nevada, and Utah: site and feature analysis. Denver, CO.Google Scholar
  9. Campbell, P. G. C., A. Hontela, J. B. Rasmussen, A. Giguère, A. Gravel, L. Kraemer, J. Kovesces, A. Lacroix, H. Levesque & G. Sherwood, 2003. Differentiating between direct (physiological) and food-chain mediated (bioenergetic) effects on fish in metal-impacted lakes. Human and Ecological Risk Assessment: An International Journal 9: 847–866.CrossRefGoogle Scholar
  10. Carlisle, D. M., 2001. Trophic structure and function of stream food webs along a gradient of metal contamination (Doctoral dissertation). Colorado State University.Google Scholar
  11. Caton, L. W., 1991. Improved subsampling methods for the EPA “Rapid Bioassessment” benthic protocols. Bulletin of the North American Benthological Society of America 8: 317–319.Google Scholar
  12. Clements, W. H., D. M. Carlisle, J. M. Lazorchak & P. C. Johnson, 2000. Heavy metals structure benthic communities in Colorado mountain streams. Ecological Applications 10: 626–638.CrossRefGoogle Scholar
  13. Clesceri, L. S., A. E. Greenberg & A. D. Eaton (eds), 1998. Standard methods for the examination of water and wastewater. Page 2-59, 20th ed. American Public Health Association, Washington, DC.Google Scholar
  14. Croteau, M.-N., S. N. Luoma & A. R. Stewart, 2005. Trophic transfer of metals along freshwater food webs: evidence of cadmium biomagnification in nature. Limnology and Oceanography 50: 1511–1519.CrossRefGoogle Scholar
  15. Currie, R. S., W. L. Fairchild & D. C. G. Muir, 1997. Remobilization and export of cadmium from lake sediments by emerging insects. Environmental Toxicology and Chemistry 16: 2333–2338.CrossRefGoogle Scholar
  16. Erickson, R. J., D. R. Mount, T. L. Highland, J. R. Hockett, E. N. Leonard, V. R. Mattson, T. D. Dawson & K. G. Lott, 2010. Effects of copper, cadmium, lead, and arsenic in a live diet on juvenile fish growth. Canadian Journal of Fisheries and Aquatic Sciences 67: 1816–1826.CrossRefGoogle Scholar
  17. Erickson, R. J., D. R. Mount, T. L. Highland, J. R. Hockett & C. T. Jenson, 2011. The relative importance of waterborne and dietborne arsenic exposure on survival and growth of juvenile rainbow trout. Aquatic Toxicology 104: 108–115.CrossRefGoogle Scholar
  18. Farag, A. M., D. F. Woodward, J. N. Goldstein, W. Brumbaugh & J. S. Meyer, 1998. Concentrations of metals associated with mining waste in sediments, biofilm, benthic macroinvertebrates, and fish from the Coeur d’Alene River basin, Idaho. Archives of Environmental Contamination and Toxicology 34: 119–127.CrossRefGoogle Scholar
  19. Farag, A. M., D. A. Nimick, B. A. Kimball, S. E. Church, D. D. Harper & W. G. Brumbaugh, 2007. Concentrations of metals in water, sediment, biofilm, benthic macroinvertebrates, and fish in the Boulder River watershed, Montana, and the role of colloids in metal uptake. Archives of Environmental Contamination and Toxicology 52: 397–409.CrossRefGoogle Scholar
  20. Feldman, D., R. Bukantis, M. Mccarthy, & D. Kron, 2012. Sample collection, sorting, taxonomic identification, and analysis of benthic macroinvertebrate communities standard operating procedure. Montana Department of Environmental Quality.Google Scholar
  21. Hansen, J. A., J. Lipton, P. G. Welsh, D. Cacela & B. MacConnell, 2009. Reduced growth of rainbow trout (Oncorhynchus mykiss) fed a live invertebrate diet pre-exposed to metal-contaminated sediments. Environmental Toxicology and Chemistry 23: 1902–1911.CrossRefGoogle Scholar
  22. Hogsden, K. L. & J. S. Harding, 2012. Consequences of acid mine drainage for the structure and function of benthic stream communities: a review. Freshwater Science 31: 108–120.CrossRefGoogle Scholar
  23. Jezierska, B. & M. Witeska, 2006. The metal uptake and accumulation in fish living in polluted waters. Soil and Water Pollution Monitoring, Protection and Remediation 3: 107–114.CrossRefGoogle Scholar
  24. Kraus, J. M., T. S. Schmidt, D. M. Walters, R. B. Wanty, R. E. Zuellig & R. E. Wolf, 2014. Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs. Ecological Applications 24: 235–243.CrossRefGoogle Scholar
  25. Langner, H., E. Greene, R. Domenech & M. Staats, 2012. Mercury and other mining-related contaminants in ospreys along the Upper Clark Fork River, Montana, USA. Archives of Environmental Contamination and Toxicology 62: 681–695.CrossRefGoogle Scholar
  26. Luoma, S. N., J. N. Moore, A. Farag, T. H. Hilman, D. J. Cain & M. Hornberger, 2008. Mining impacts on fish in the Clark Fork river, Montana: a field ecotoxicology case study. Page 1071. In Di Giulio, R. T. & D. E. Hinton (eds), Toxicology of Fishes. CRC Press, Boca Raton, FL.Google Scholar
  27. MacDonald, D. D., C. G. Ingersoll & T. A. Berger, 2000. Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Archives of Environmental Contamination and Toxicology 39: 20–31.CrossRefGoogle Scholar
  28. Mebane, C. A., R. J. Eakins, B. G. Fraser & W. J. Adams, 2015. Recovery of a mining-damaged stream ecosystem. Elementa: science of the Anthropocene 3: 42.Google Scholar
  29. Menzie, C. A., 1980. Potential significance of insects in the removal of contaminants from aquatic systems. Water, Air, and Soil Pollution 13: 473–479.CrossRefGoogle Scholar
  30. Monna, F., E. Camizuli, P. Revelli, C. Biville, C. Thomas, R. Losno, R. Scheifler, O. Bruguier, S. Baron, C. Chateau, A. Ploquin & P. Alibert, 2011. Wild brown trout affected by historical mining in the Cevennes National Park, France. Environmental Science and Technology 45: 6823–6830.CrossRefGoogle Scholar
  31. Montana Department of Environmental Quality, 2016. Record of Decision. Final Cleanup for the Upper Blackfoot Mining Complex State Superfund Facility, Lewis and Clark County.Google Scholar
  32. Montana Fish Wildlife and Parks, 1997. Effects of the June, 1975 Mike Horse Mine Tailings Dam failure on water quality and aquatic resources of the Upper Blackfoot River. Montana, Helena, MT.Google Scholar
  33. Moore, J. N. & H. W. Langner, 2012. Can a river heal itself? Natural attenuation of metal contamination in river sediment. Environmental Science & Technology 46: 2616–2623.CrossRefGoogle Scholar
  34. Moore, J. N., S. N. Luoma & D. Peters, 1991. Downstream effects of mine effluent on an intermontane riparian system. Canadian Journal of Fisheries and Aquatic Sciences 48: 222–232.CrossRefGoogle Scholar
  35. Nagorski, S. A., J. N. Moore & D. B. Smith, 2002a. Distribution of Metals in Water and Bed Sediment in a Mineral-Rich Watershed, Montana, USA. Mine Water and the Environment 21: 121–136.CrossRefGoogle Scholar
  36. Nagorski, S. A., J. N. Moore & D. B. Smith, 2002b. Distribution of metals in water and bed sediment in a mineral-rich watershed, Montana, USA. Mine Water and the Environment 21: 121–136.CrossRefGoogle Scholar
  37. Nakano, S., K. D. Fausch, T. Furukawa-Tanaka, K. Maekawa & H. Kawanabe, 1992. Resource utilization by bull char and cutthroat trout in a mountain stream in Montana, U.S.A. Japanese Journal of Ichthyology 39: 211–217.Google Scholar
  38. Newman, R. M., 1987. Comparison of encounter model predictions with observed size-selectivity by stream trout. Journal of North American Benthological Society 6: 56–64.CrossRefGoogle Scholar
  39. Poff, N. L., J. D. Olden, N. K. M. Vieira, D. S. Finn, M. P. Simmons & B. C. Kondratieff, 2006. Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. Journal of the North American Benthological Society 25: 730–755.CrossRefGoogle Scholar
  40. Poulton, B. C., D. P. Monda, D. F. Woodward, M. L. Wildhaber & W. G. Brumbaugh, 1995. Relations between benthic community structure and metals concentrations in aquatic macroinvertebrates: Clark Fork River, Montana. Journal of Freshwater Ecology 10: 277–293.CrossRefGoogle Scholar
  41. Quinn, M. R., X. Feng, C. L. Folt & C. P. Chamberlain, 2003. Analyzing trophic transfer of metals in stream food webs using nitrogen isotopes. Science of the Total Environment 317: 73–89.CrossRefGoogle Scholar
  42. R Core Team, 2015. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, https://www.r-project.org/.
  43. Rader, R. B., 1997. A functional classification of the drift: traits that influence invertebrate availability to salmonids. Canadian Journal of Fisheries and Aquatic Sciences 54: 1211–1234.CrossRefGoogle Scholar
  44. Schemel, L. E., B. A. Kimball & K. E. Bencala, 2000. Colloid formation and metal transport through two mixing zones affected by acid mine drainage near Silverton, Colorado. Applied Geochemistry 15: 1003–1018.CrossRefGoogle Scholar
  45. Schmitz, D., J. Mason, M. Blank, & J. Cahoon, 2010. Channel response assessment for the upper Blackfoot River. Montana Department of Natural Resources and Conservation 1–46.Google Scholar
  46. Shelton, L. R., & P. D. Capel, 1994. Guidelines for collecting and processing samples of stream bed sediment for analysis of trace elements and organic contaminants for the National Water-Quality Assessment Program. US Geological Survey Open-File Report 94–458, Sacramento, California.Google Scholar
  47. Song, J., X. Yang, J. Zhang, Y. Long, Y. Zhang & T. Zhang, 2015. Assessing the variability of heavy metal concentrations in liquid-solid two-phase and related environmental risks in the Weihe River of Shaanxi Province, China. International Journal of Environmental Research and Public Health 12: 8243–8262.CrossRefGoogle Scholar
  48. U.S. Environmental Protection Agency, 1991. Methods for the determination of metals in environmental samples. Washington, DC.Google Scholar
  49. U.S. Environmental Protection Agency, 2007. Aquatic Life Ambient Freshwater Quality Criteria – Copper. Washington, DC.Google Scholar
  50. U.S. Environmental Protection Agency, 2016. Aquatic Life Ambient Water Quality Criteria – Cadmium. Washington, DC.Google Scholar
  51. U.S. Fish and Wildlife Service, 1993. Milltown endangerment assessment project: effects of metal-contaminated sediment, water, and diet on aquatic organisms. National Fisheries Contaminant Research Center, Columbia, MO.Google Scholar
  52. Vandeberg, G. S., C. W. Martin & G. M. Pierzynski, 2011. Spatial distribution of trace elements in floodplain alluvium of the upper Blackfoot River, Montana. Environmental Earth Sciences 62: 1521–1534.CrossRefGoogle Scholar
  53. Ward, J. V. & B. C. Kondratieff, 1992. An illustrated guide to the mountain stream insects of Colorado. University Press of Colorado, Fort Collins.Google Scholar
  54. Wolman, G. M., 1954. A method of sampling coarse river-bed material. Transactions of the American Geophysical Union 35: 951–956.CrossRefGoogle Scholar
  55. Woodward, D. F., W. G. Brumbaugh, A. J. Lelonay, E. E. Little & C. Smith, 1994. Effects on rainbow trout fry of a metals-contaminated diet of benthic invertebrates from the Clark Fork River, Montana. Transactions of the American Fisheries Society 123: 51–62.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Environmental Studies ProgramUniversity of MontanaMissoulaUSA
  2. 2.Rhithron Associates IncMissoulaUSA
  3. 3.Department of Ecosystem and Conservation SciencesUniversity of MontanaMissoulaUSA
  4. 4.Department of GeosciencesUniversity of MontanaMissoulaUSA
  5. 5.King Abdullah University of Science and TechnologyThuwalSaudi Arabia

Personalised recommendations