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Hydrobiologia

, Volume 784, Issue 1, pp 225–236 | Cite as

Extracellular enzyme activity suggests phosphorus limitation of biofilm productivity in acid mine drainage remediated streams

  • Samuel A. DrerupEmail author
  • Morgan L. Vis
Primary Research Paper

Abstract

Acid mine drainage (AMD) is a global consequence of historical and present day mining activities. Remediation efforts have been successful in improving water quality with elevated pH and decreased dissolved metals. In many streams, there has been chemical and biological recovery, but success is not universal. The goal of restoration should be to improve not only biological diversity but also stream function. We compared biofilm community characteristics and function from three stream categories (AMD-unimpaired, AMD-impaired, and AMD-remediated) in southeastern Ohio. Biofilms of the AMD-impaired and AMD-remediated sites had the lowest concentrations of chlorophyll a and the lowest rates of productivity and respiration. AMD-impaired streams had reduced pH and increased dissolved metal (iron, aluminum, and manganese) concentrations. Specific conductance was elevated in both the AMD-impaired and AMD-remediated streams. Water at the AMD-impacted and AMD-remediated sites had significantly lower soluble reactive phosphorus concentration compared to AMD-unimpaired sites. Biofilm extracellular enzyme activities showed an increase in biomass-specific phosphorus-acquiring enzymes in AMD-impaired and AMD-remediated sites. These results suggest phosphorus limitation is occurring in AMD-impaired and AMD-remediated streams, potentially limiting or delaying biotic recovery even though water chemistry has improved.

Keywords

Acid mine drainage Extracellular enzyme activity Phosphorus limitation Primary productivity Remediation 

Notes

Acknowledgments

We would like to thank Jessica Lindner for her assistance in collecting field samples and laboratory analysis. Sites used in this study were selected with the assistance of Jen Bowman (Voinovich School of Leadership and Public Affairs, Ohio University) and Kelly Johnson (Biological Sciences, Ohio University). Comments provided by Jared Deforest, Kelly Johnson, Brian McCarthy, and two anonymous reviewers greatly enhanced the quality of this manuscript. An Ohio University Graduate Student Senate Original Works Grant and an Ohio University Student Enhancement Award provided funding for the research. SD received assistantship support from the American Energy Power Foundation Graduate Assistantship for Watershed Assessment and Restoration awarded through the Voinovich School of Leadership and Public Affairs.

References

  1. Baker, B. J. & J. F. Banfield, 2003. Microbial communities in acid mine drainage. FEMS Microbiology Ecology 44: 139–152.CrossRefPubMedGoogle Scholar
  2. Bott, T. L., J. K. Jackson, M. E. McTammany, J. D. Newbold, S. T. Rier, B. W. Sweeney & J. M. Battle, 2012. Abandoned coal mine drainage and its remediation: impacts on stream ecosystem structure and function. Ecological Applications 22: 2144–2163.CrossRefPubMedGoogle Scholar
  3. Bowman, J. R. & K. S. Johnson, 2015. An Evaluation of Water Quality, Biology, and Acid mine drainage reclamation in five watersheds: Raccoon Creek, Monday Creek, Sunday Creek, Huff Run, and Leading Creek, Voinovich School of Leadership and Public Affairs, Ohio University, http://watersheddata.com/userview_file.aspx?UserFileLo=1&UserFileID=173.
  4. Crossey, M. J. & T. W. L. Point, 1988. A comparison of periphyton community structural and functional responses to heavy metals. Hydrobiologia 162: 109–121.CrossRefGoogle Scholar
  5. DeNicola, D. M. & A. J. Lellock, 2015. Nutrient limitation of algal periphyton in streams along an acid mine drainage gradient. Journal of Phycology 51: 739–749.CrossRefPubMedGoogle Scholar
  6. DeNicola, D. M. & M. G. Stapleton, 2014. Benthic diatoms as indicators of long-term changes in a watershed receiving passive treatment for acid mine drainage. Hydrobiologia 732: 29–48.CrossRefGoogle Scholar
  7. DeNicola, D. M., L. Layton & T. R. Czapski, 2012. Epilithic community metabolism as an indicator of impact and recovery in streams affected by acid mine drainage. Environmental Management 50: 1035–1046.CrossRefPubMedGoogle Scholar
  8. Gray, N. F., 1997. Environmental impact and remediation of acid mine drainage: a management problem. Environmental Geology 30: 62–71.CrossRefGoogle Scholar
  9. Gray, J. B. & M. L. Vis, 2013. Reference diatom assemblage response to restoration of an acid mine drainage stream. Ecological Indicators 29: 234–245.CrossRefGoogle Scholar
  10. Gunn, J., C. Sarrazin-Delay, B. Wesolek, A. Stasko & E. Szkokan-Emilson, 2010. Delayed recovery of Benthic Macroinvertebrate Communities in junction Creek, Sudbury, Ontario, after the diversion of acid mine drainage. Human and Ecological Risk Assessment 16: 901–912.CrossRefGoogle Scholar
  11. Hill, B. H., J. M. Lazorchak, F. H. McCormick & W. T. Willingham, 1997. The effects of elevated metals on benthic community metabolism in a Rocky Mountain stream. Environmental Pollution 95: 183–190.CrossRefPubMedGoogle Scholar
  12. Hill, B. H., C. M. Elonen, T. M. Jicha, D. W. Bolgrien & M. F. Moffett, 2009. Sediment microbial enzyme activity as an indicator of nutrient limitation in the great rivers of the Upper Mississippi River basin. Biogeochemistry 97: 195–209.CrossRefGoogle Scholar
  13. Hill, B. H., F. H. McCormick, B. C. Harvey, S. L. Johnson, M. L. Warren & C. M. Elonen, 2010. Microbial enzyme activity, nutrient uptake and nutrient limitation in forested streams. Freshwater Biology 55: 1005–1019.CrossRefGoogle Scholar
  14. Hill, B. H., C. M. Elonen, L. R. Seifert, A. A. May & E. Tarquinio, 2012. Microbial enzyme stoichiometry and nutrient limitation in US streams and rivers. Ecological Indicators 18: 540–551.CrossRefGoogle Scholar
  15. Hill, B. H., C. M. Elonen, T. M. Jicha, R. K. Kolka, L. L. P. Lehto, S. D. Sebestyen & L. R. Seifert-Monson, 2014. Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatland types. Biogeochemistry 120: 203–224.CrossRefGoogle Scholar
  16. 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
  17. Hogsden, K. L. & J. S. Harding, 2013. Leaf breakdown, detrital resources, and food webs in streams affected by mine drainage. Hydrobiologia 716: 59–73.CrossRefGoogle Scholar
  18. Johnson, K. S., 2009. Performance of a family-level macroinvertebrate index (MAIS) for assessing acid mine impacts on streams in the Western Allegheny Plateau. Ohio University.Google Scholar
  19. Johnson, D. B. & K. B. Hallberg, 2005. Acid mine drainage remediation options: a review. Science of the Total Environment 338: 3–14.CrossRefPubMedGoogle Scholar
  20. Johnson, K. S., P. C. Thompson, L. Gromen & J. Bowman, 2014. Use of leaf litter breakdown and macroinvertebrates to evaluate gradient of recovery in an acid mine impacted stream remediated with an active alkaline doser. Environmental Monitoring and Assessment 186: 4111–4127.CrossRefPubMedGoogle Scholar
  21. Kleinmann, R. L., B. Hornberger, B. Leavitt & D. M. Hyman, 2000. Introduction and recomendations prediction of water quality at surface coal mines. National Mine Land Reclamation Center, West Virginia University, Mrgantown, W. Va.: 1–7.Google Scholar
  22. Kruse, N. A., J. R. Bowman, A. L. Mackey, B. McCament & K. S. Johnson, 2012. The lasting impacts of offline periods in lime dosed streams: a case study in Raccoon Creek, Ohio. Mine Water and the Environment 31: 266–272.CrossRefGoogle Scholar
  23. Lear, G., D. Niyogi, J. Harding, Y. Dong & G. Lewis, 2009. Biofilm bacterial community structure in streams affected by acid mine drainage. Applied and Environmental Microbiology 75: 3455–3460.CrossRefPubMedPubMedCentralGoogle Scholar
  24. McClurg, S. E., J. T. Petty, P. M. Mazik & J. L. Clayton, 2007. Stream ecosystem response to limestone treatment in acid impacted watersheds of the Allegheny Plateau. Ecological Applications 17: 1087–1104.CrossRefPubMedGoogle Scholar
  25. Neculita, C.-M., G. J. Zagury & B. Bussière, 2007. Passive treatment of acid mine drainage in bioreactors using sulfate-reducing bacteria. Journal of Environment Quality 36: 1.CrossRefGoogle Scholar
  26. Niyogi, D. K., D. M. McKnight & W. M. Lewis Jr., 1999. Influences of water and substrate quality for periphyton in a montane stream affected by acid mine drainage. Limnology and Oceanography 44: 804–809.CrossRefGoogle Scholar
  27. Niyogi, D. K., W. M. Lewis Jr. & D. M. McKnight, 2002a. Effects of strees from mine drainage on diversity, biomass, and function of primary producers in mountain streams. Ecosystems 5: 554–567.Google Scholar
  28. Niyogi, D. K., D. M. McKnight & W. M. Lewis Jr., 2002b. Fungal Communities and biomass in mountain streams affected by mine drainage. Archive fur Hydrobiologie 155: 255–271.CrossRefGoogle Scholar
  29. Niyogi, D. K., J. S. Harding & K. S. Simon, 2013. Organic matter breakdown as a measure of stream health in New Zealand streams affected by acid mine drainage. Ecological Indicators 24: 510–517.CrossRefGoogle Scholar
  30. Northington, R. M., E. F. Benfield, S. H. Schoenholtz, A. J. Timpano, J. R. Webster & C. Zipper, 2011. An assessment of structural attributes and ecosystem function in restored Virginia coalfield streams. Hydrobiologia 671: 51–63.CrossRefGoogle Scholar
  31. OEPA, 1987. 3745-1-07: Water use designations and statewide criteria. State of Ohio.Google Scholar
  32. Palmer, M. A., R. F. Ambrose & N. L. Poff, 1997. Ecological theory and community restoration ecology. Restoration Ecology 5: 291–300.CrossRefGoogle Scholar
  33. Pool, J. R., N. A. Kruse & M. L. Vis, 2013. Assessment of mine drainage remediated streams using diatom assemblages and biofilm enzyme activities. Hydrobiologia 709: 101–116.CrossRefGoogle Scholar
  34. R Core Team, 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
  35. Rier, S. T., K. A. Kuehn & S. N. Francoeur, 2007. Algal regulation of extracellular enzyme activity in stream microbial communities associated with inert substrata and detritus. Journal of the North American Benthological Society 26: 439–449.CrossRefGoogle Scholar
  36. Rosemond, A. D., P. J. Mulholland & J. W. Elwood, 1993. Top-down and bottom-up control of stream periphyton: effects of nutrients and herbivores. Ecology 74: 1264–1280.CrossRefGoogle Scholar
  37. Ryder, D. S. & W. Miller, 2005. Setting goals and measuring success: linking patterns and processes in stream restoration. Hydrobiologia 552: 147–158.CrossRefGoogle Scholar
  38. Schowe, K. & J. Harding, 2014. Development of two diatom-based indices: a biotic and a multimetric index for assessing mine impacts in New Zealand streams. New Zealand Journal of Marine and Freshwater Research 48: 163–176.CrossRefGoogle Scholar
  39. Shelley, T. E., 1979. The effect of rock size upon the distribution of species of Orthocladiinae (Chironomidae: Diptera) and Baetis intercalasis. McDonnaugh (Baetidae: Ephemeroptera). Ecol. Entomol. 4: 95–100.Google Scholar
  40. Simmons, J. A., 2010. Phosphorus removal by sediment in streams contaminated with acid mine drainage. Water, Air, & Soil Pollution 209: 123–132.CrossRefGoogle Scholar
  41. Sinsabaugh, R. L. & J. J. F. Shah, 2012. Ecoenzymatic stoichiometry and ecological theory. Annual Review of Ecology, Evolution, and Systematics 43: 313–343.CrossRefGoogle Scholar
  42. Sinsabaugh, R. L., J. Belnap, S. G. Findlay, J. J. F. Shah, B. H. Hill, K. A. Kuehn, C. R. Kuske, M. E. Litvak, N. G. Martinez, D. L. Moorhead & D. D. Warnock, 2014. Extracellular enzyme kinetics scale with resource availability. Biogeochemistry 121: 287–304.CrossRefGoogle Scholar
  43. Smith, E. & J. R. Voshell, 1997. Studies of Benthic Macroinvertebrates and Fish in Streams Within EPA Region 3 for Development of Biological Indicators of Ecological Condition. Virginia Polytechnic Institute and State University, Blacksburg, Virginia, http://www.epa.state.oh.us/portals/35/volunteermonitoring/references/SmithandVoshell1997.pdf.
  44. Smucker, N. J. & M. L. Vis, 2009. Use of diatoms to assess agricultural and coal mining impacts on streams and a multiassemblage case study. Journal of the North American Benthological Society 28: 659–675.CrossRefGoogle Scholar
  45. Smucker, N. J., J. L. DeForest & M. L. Vis, 2009. Different methods and storage duration affect measurements of epilithic extracellular enzyme activities in lotic biofilms. Hydrobiologia 636: 153–162.Google Scholar
  46. Smucker, N. J. & M. L. Vis, 2011. Acid mine drainage affects the development and function of epilithic biofilms in streams. Journal of the North American Benthological Society 30: 728–738.CrossRefGoogle Scholar
  47. Smucker, N. J., S. A. Drerup & M. L. Vis, 2014. Roles of benthic algae in the structure, function, and assessment of stream ecosystems affected by acid mine drainage. Journal of Phycology 50: 425–436.CrossRefPubMedGoogle Scholar
  48. Stainton, M.P., M.J. Capel & F.A. Armstrong, 1974. The chemical analysis of fresh water. Department of the Environment (Canada). Fisheries and Marine Service. Miscellaneous special publication No. 25.Google Scholar
  49. Tate, C. M., R. E. Broshears & D. M. McKnight, 1995. Phosphate dynamics in an acidic mountain stream: interactions involving algal uptake, sorption by iron oxide, and photoreduction. Limnology and Oceanography 40: 938–946.CrossRefGoogle Scholar
  50. Underwood, B. E., N. A. Kruse & J. R. Bowman, 2014. Long-term chemical and biological improvement in an acid mine drainage-impacted watershed. Environmental Monitoring and Assessment 1–15.Google Scholar
  51. Wei, X., R. C. Viadero Jr. & S. Bhojappa, 2008. Phosphorus removal by acid mine drainage sludge from secondary effluents of municipal wastewater treatment plants. Water Research 42: 3275–3284.CrossRefPubMedGoogle Scholar
  52. Zalack, J. T., N. J. Smucker & M. L. Vis, 2010. Development of a diatom index of biotic integrity for acid mine drainage impacted streams. Ecological Indicators 10: 287–295.CrossRefGoogle Scholar
  53. Ziemkiewicz, P. F., J. G. Skousen & J. Simmons, 2003. Long-term performance of passive acid mine drainage treatment systems. Mine Water and the Environment 22: 118–129.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Environmental and Plant BiologyOhio UniversityAthensUSA

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