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Estuaries and Coasts

, Volume 35, Issue 6, pp 1453–1467 | Cite as

Using δ15N in Fish Larvae as an Indicator of Watershed Sources of Anthropogenic Nitrogen: Response at Multiple Spatial Scales

  • Joel C. HoffmanEmail author
  • John R. Kelly
  • Greg S. Peterson
  • Anne M. Cotter
  • Matthew A. Starry
  • Michael E. Sierszen
Article

Abstract

There is growing interest in applying δ15N in biota as an indicator of anthropogenic nutrient inputs to coastal environments because changes in δ15N correlate to inputs of land-based nutrients. In complex coastal receiving waters, however, land-use effects on biota δ15N may be masked by local hydrologic processes, especially exchange with coastal waters of different geochemical character. We examined δ15N differences among larval fish, a novel biotic indicator, in coastal receiving waters at both among and within watershed scales. Our goal was to characterize how hydrologic processes within coastal river mouths and embayments mediate the effect of land-based N sources on larval fish δ15N. We sampled three Lake Superior river-embayment systems from watersheds that span a large population density gradient. Over all stations, mean fish δ15N ranged from 2.7 ‰ to 10.8 ‰. Within each system, we found a different pattern in δ15N across the river–lake transition zone. Correlations between fish δ15N and water quality, particularly NH 4 + and total nitrogen, were highly significant and corresponded to known differences in sewage waste water inputs. A multivariate model that included both watershed-based population density and NH 4 + was found to provide the best fit to the δ15N data among a series of multi- and univariate candidate models. These results demonstrate that: (1) fish larvae δ15N responded at within watershed scales, and (2) within coastal receiving waters, fish larvae δ15N was related to waste water inputs at the watershed scale; however, expression at specific locations within a coastal system was strongly influenced by local hydrologic processes.

Keywords

Nitrogen stable isotopes Eutrophication Monitoring Sewage waste water Great Lakes 

Notes

Acknowledgments

We thank T. Corry, J. Van Alstine, M. Pearson, A. Trebitz, and C. Butterworth for field assistance; A. Just, L. Seifert, and M. Knuth for laboratory assistance; and A. Oczkowski and two anonymous reviewers for helpful comments on the manuscript. The views expressed in this paper are those of the authors and do not necessarily reflect the views or policies of the US EPA.

References

  1. Anderson, C., and G. Cabana. 2005. δ15N in riverine food webs: effects of N inputs from agricultural watersheds. Canadian Journal of Fisheries and Aquatic Sciences 62: 333–340.CrossRefGoogle Scholar
  2. Bannon, R.O., and C.T. Roman. 2008. Using stable isotope to monitor anthropogenic nitrogen inputs to estuaries. Ecological Applications 18: 22–30.CrossRefGoogle Scholar
  3. Bedard-Haughn, A., J.W. van Groenigen, and C. van Kessel. 2003. Tracing 15N through landscapes: potential uses and precautions. Journal of Hydrology 272: 175–190.CrossRefGoogle Scholar
  4. Cabana, G., and J.B. Rasmussen. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Sciences 93: 10844–10847.CrossRefGoogle Scholar
  5. Cifuentes, L.A., J.H. Sharp, and M.L. Fogel. 1988. Stable carbon and nitrogen isotope biogeochemistry in the Delaware estuary. Limnology and Oceanography 33: 1102–1115.CrossRefGoogle Scholar
  6. Cohen, R.A., and P. Fong. 2006. Using opportunistic green macroalgae as indicators of nitrogen supply and sources to estuaries. Ecological Applications 16: 1405–1420.CrossRefGoogle Scholar
  7. Cole, M.L., I. Valiela, K.D. Kroeger, G.L. Tomasky, J. Cebrian, C. Wigand, R.A. McKinney, S.P. Grady, and M.H. Carvalho da Silva. 2004. Assessment of a δ15N isotopic method to indicate anthropogenic eutrophication in aquatic ecosystems. Journal of Environmental Quality 33: 124–132.CrossRefGoogle Scholar
  8. Diaz, R.J., and R. Rosenberg. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321: 926–929.CrossRefGoogle Scholar
  9. Diebel, M.W., and M.J. Vander Zanden. 2009. Nitrogen stable isotope n streams: effects of agricultural sources and transformations. Ecological Applications 19: 1127–1134.CrossRefGoogle Scholar
  10. Elliott, E.M., and G.S. Brush. 2006. Sedimented organic nitrogen isotopes in freshwater wetlands record long-term changes in watershed nitrogen source and land use. Environmental Science and Technology 40: 2910–2916.CrossRefGoogle Scholar
  11. Fertig, B., T.J.B. Carruthers, W.C. Dennison, A.B. Jones, F. Pantus, and B. Longstaff. 2009. Oyster and macroalgae bioindicators detect elevated δ15N in Maryland’s coastal bays. Estuaries and Coasts 32: 773–786.CrossRefGoogle Scholar
  12. Feuchtmayer, H., and J. Grey. 2003. Effect of preparation and preservation procedures on carbon and nitrogen stable isotope determinations from zooplankton. Rapid Communications in Mass Spectrometry 17: 2605–2610.CrossRefGoogle Scholar
  13. Finlay, J.C., R.W. Sterner, and S. Kumar. 2007. Isotopic evidence for in-lake production of accumulating nitrate in Lake Superior. Ecological Applications 17: 2323–2332.CrossRefGoogle Scholar
  14. Fry, B. 1999. Using stable isotopes to monitor watershed influences on aquatic trophodynamics. Canadian Journal of Fisheries and Aquatic Sciences 56: 2167–2171.CrossRefGoogle Scholar
  15. Gartner, A., P. Lavery, and A.J. Smith. 2002. Use of δ15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal. Marine Ecology Progress Series 235: 63–73.CrossRefGoogle Scholar
  16. Harrington, R.R., B.P. Kennedy, C.P. Chamberlain, J.D. Blum, and C.L. Folt. 1998. 15N enrichment in agricultural catchments: field patterns and applications to tracking Atlantic salmon (Salmo salar). Chemical Geology 147: 281–294.CrossRefGoogle Scholar
  17. Hesslein, R.H., K.A. Hallard, and P. Ramlal. 1993. Replacement of sulfur, carbon, and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50: 2071–2076.CrossRefGoogle Scholar
  18. Hoffman, J.C., D.A. Bronk, and J.E. Olney. 2007. Tracking nursery habitat use by young American shad in the York River estuary, Virginia using stable isotopes. Transactions of the American Fisheries Society 136: 1285–1297.CrossRefGoogle Scholar
  19. Hoffman, J.C., A.M. Cotter, G.S. Peterson, and J.R. Kelly. 2010. Using stable isotope mixing in a Great Lakes coastal tributary to determine food web linkages in young fishes. Estuaries and Coasts 33: 1391–1405.CrossRefGoogle Scholar
  20. Hoffman, J.C., A.M. Cotter, G.S. Peterson, T.D. Corry, and J.R. Kelly. 2011. Rapid stable isotope turnover of larval fish in a Lake Superior coastal wetland: implications for diet and life history studies. Aquatic Ecosystem Health and Management 14: 403–413.CrossRefGoogle Scholar
  21. Kaldy, J. 2011. Using a macroalgal δ15N bioassay to detect cruise ship waste water effluent inputs. Marine Pollution Bulletin 62: 1762–1771.CrossRefGoogle Scholar
  22. Karube, Z., Y. Sakai, T. Takeyama, N. Okuda, A. Kohzu, C. Yoshimizu, T. Nagata, and I. Tayasu. 2010. Carbon and nitrogen stable isotope ratios of macroinvertebrates in the littoral zone of Lake Biwa as indicators of anthropogenic activities in the watershed. Ecological Research 25: 847–855.CrossRefGoogle Scholar
  23. Kelly, J.R. 2008. Chapter 10: nitrogen effects on coastal marine ecosystems. In Nitrogen in the environment: sources, problems, and management, 2nd ed, ed. J.L. Hatfield and R.F. Follett, 271–332. Amsterdam: Elsevier.Google Scholar
  24. Kendall, C., E.M. Elliott, and S.D. Wankel. 2007. Tracing anthropogenic inputs of nitrogen to ecosystems, Chapter 12. In: Stable isotopes in ecology and environmental science, 2nd edition, eds. Michener, R.H., and K. Lajtha, pp. 375–449. Blackwell Publishing. Pittsburg, PNGoogle Scholar
  25. Knuth, M.L., and J.R. Kelly. 2011. Denitrification rates in a Lake Superior coastal wetland. Aquatic Ecosystem Health and Management 14: 414–421.CrossRefGoogle Scholar
  26. Kohzu, A., T. Miyajima, I. Tayasu, C. Yoshimizu, F. Hyodo, K. Matsui, T. Nakano, E. Wada, N. Fujita, and T. Nagata. 2008. Use of stable nitrogen isotope signatures of riparian macrophytes as an indicator of anthropogenic N inputs to river ecosystems. Environmental Science and Technology 42: 7387–7841.CrossRefGoogle Scholar
  27. Kohzu, A., I. Tayasu, C. Yoshimizu, A. Maruyama, Y. Kohmatsu, F. Hyodo, Y. Onoda, A. Igeta, K. Matsui, T. Nakano, E. Wada, T. Nagata, and Y. Takemon. 2009. Nitrogen stable isotopic signatures of basal food items, primary consumers and omnivores in rivers with different levels of human impact. Ecological Research 24: 127–136.CrossRefGoogle Scholar
  28. Lake, J.L., R.A. McKinney, F.A. Osterman, R.J. Pruell, J. Kiddon, S.A. Ryba, and A.D. Libby. 2001. Stable nitrogen isotopes as indicators of anthropogenic activities in small freshwater systems. Canadian Journal of Fisheries and Aquatic Sciences 58: 870–878.CrossRefGoogle Scholar
  29. Leavitt, P.R., C.S. Brock, C. Ebel, and A. Patoine. 2006. Landscape-scale effects of urban nitrogen on a chain of freshwater lakes in central North America. Limnology and Oceanography 51: 2262–2277.CrossRefGoogle Scholar
  30. Lefebvre, S., J.-C. Clément, G. Pinay, C. Thenail, P. Durand, and P. Marmonier. 2007. 15N-nitrate signature in low-order streams: effects of land cover and agricultural practices. Ecological Applications 17: 2333–2346.CrossRefGoogle Scholar
  31. Logan, J., H. Haas, L. Deegan, and E. Gaines. 2006. Turnover rates of nitrogen stable isotopes in the salt marsh mummichog, Fundulus heteroclitus, following a laboratory diet switch. Oecologia 147: 391–395.CrossRefGoogle Scholar
  32. Mayer, B., E.W. Boyer, C. Goodale, N.A. Jaworski, N. Van Breemen, R.B. Howarth, S. Seitzinger, G. Billen, K. Lajtha, K. Nadelhoffer, D. Van Dam, L.J. Hetling, M. Nosal, and K. Paustian. 2002. Sources of nitrate in rivers draining sixteen watersheds in the northeastern U.S.: isotopic constraints. Biogeochemistry 57(58): 171–197.CrossRefGoogle Scholar
  33. McClelland, J.W., and I. Valiela. 1998. Linking nitrogen in estuarine producers to land-derived sources. Limnology and Oceanography 43: 577–585.CrossRefGoogle Scholar
  34. McKinney, R.A., W.G. Nelson, M.A. Charpentier, and C. Wigand. 2001. Ribbed mussel nitrogen isotope signatures reflect nitrogen sources in coastal salt marshes. Ecological Applications 11: 203–214.CrossRefGoogle Scholar
  35. McKinney, R.A., J.L. Lake, M.A. Charpentier, and S. Ryba. 2002. Using mussel isotope ratios to assess anthropogenic nitrogen inputs to freshwater ecosystems. Environmental Monitoring and Assessment 74: 167–192.CrossRefGoogle Scholar
  36. Morrice, J.A., A.S. Trebitz, J.R. Kelly, A.M. Cotter, and M.L. Knuth. 2009. Nutrient variability in Lake Superior coastal wetlands: the role of land use and hydrology. In The state of Lake Superior, ed. M. Munawar and I.F. Munawar, 217–238. Burlington: Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society Ecovision Series.Google Scholar
  37. Murchie, K.J., and M. Power. 2004. Growth- and feeding-related isotopic dilution and enrichment patterns in young-of-the-year yellow perch (Perca flavescens). Freshwater Biology 49: 41–54.CrossRefGoogle Scholar
  38. Niemi, G.J., E.D. Reavie, G.S. Peterson, J.R. Kelly, C.A. Johnston, L.B. Johnson, R.W. Howe, G.E. Host, T.P. Hollenhorst, N.P. Danz, J.J.H. Ciborowski, T.N. Brown, V.J. Brady, and R.P. Axler. 2011. An integrated approach to assessing multiple stressors for coastal Lake Superior. Aquatic Ecosystem Health and Management 14: 356–375.CrossRefGoogle Scholar
  39. Oczkowski, A., S. Nixon, K. Henry, P. DiMilla, M. Pilson, S. Granger, B. Buckley, C. Thornber, R. McKinney, and J. Chaves. 2008. Distribution and trophic importance of anthropogenic nitrogen in Narragansett Bay: an assessment using stable isotopes. Estuaries and Coasts 31: 53–69.CrossRefGoogle Scholar
  40. Page, H.M. 1995. Variation in the natural abundance of 15N in the halophyte, Salicornia virginica, associated with groundwater subsidies of nitrogen in a southern California salt-marsh. Oecologia 104: 181–188.CrossRefGoogle Scholar
  41. Peterson, G.S., M.E. Sierszen, P.M. Yurista, and J.R. Kelly. 2007. Stable nitrogen isotopes of plankton and benthos reflect a landscape-level influences on Great Lakes coastal ecosystems. Journal of Great Lakes Research 33(SI 3): 27–41.CrossRefGoogle Scholar
  42. Phillips, D.L., and J.W. Gregg. 2003. Source partitioning using stable isotopes: coping with too many sources. Oecologia 136: 261–269.CrossRefGoogle Scholar
  43. Savage, C., and R. Elmgren. 2004. Macroalgal (Fucus vesiculosus) δ15N values trace decrease in sewage influence. Ecological Applications 14: 517–526.CrossRefGoogle Scholar
  44. Schlacher, T.A., B. Liddell, T.F. Gaston, and M. Schlacher-Hoenlinger. 2005. Fish track waste water pollution to estuaries. Oecologia 144: 570–584.CrossRefGoogle Scholar
  45. Sierszen, M.E., J.C. Brazner, A.M. Cotter, J.A. Morrice, G.S. Peterson, and A.S. Trebitz. 2012. Watershed and lake influences on the energetic base of coastal wetland food webs across the Great Lakes Basin. Journal of Great Lakes Research (in press).Google Scholar
  46. Steffy, L., and S.S. Kilham. 2004. Elevated δ15N in stream biota in areas with septic tank systems in an urban watershed. Ecological Applications 14: 637–641.CrossRefGoogle Scholar
  47. Umezawa, Y., T. Miyajima, M. Yamamuro, H. Kayanne, and I. Koiki. 2002. Fine-scale mapping of land-derived nitrogen in coral reefs by δ15N in macroalgae. Limnology and Oceanography 47: 1405–1416.CrossRefGoogle Scholar
  48. U.S. EPA. 1983. Methods for chemical analyses of waters and wastes. U.S. Environmental Protection Agency, Cincinnati, Ohio. EPA/600/4-79/020.Google Scholar
  49. U.S. EPA. 1991. The determination of inorganic anions in water by ion chromatography. U.S. Environmental Protection Agency, Cincinnati, Ohio. Environmental Monitoring Systems Laboratory Method 300.0.Google Scholar
  50. U.S. EPA. 1993. Methods for determination of inorganic substances in environmental samples. U.S. Environ mental Protection Agency, Cincinnati, Ohio. EPA/600/R-93/100.Google Scholar
  51. Vander Zanden, M.J., and J.B. Rasmussen. 2001. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnology and Oceanography 46: 2061–2066.Google Scholar
  52. Vander Zanden, J., Y. Vadeboncoeur, M. Diebel, and E. Jeppesen. 2005. Primary consumer stable nitrogen isotopes as indicators of nutrient source. Environmental Science and Technology 39: 7509–7515.CrossRefGoogle Scholar
  53. Viana, I.G., J.A. Fernández, J.R. Aboal, and A. Carballeira. 2011. Measurement of δ15N in macroalgae stored in an environmental specimen bank for regional scale monitoring of eutrophication in coastal areas. Ecological Indicators 11: 888–895.CrossRefGoogle Scholar
  54. Yurista, P.M., and J.R. Kelly. 2009. Spatial patterns of water quality and plankton from high-resolution continuous in situ sensing along a 537-km nearshore transect of western Lake Superior, 2004. In The state of Lake Superior, ed. M. Munawar and I.F. Munawar, 439–471. Burlington: Ecovision World Monograph Series, Aquatic Ecosystem Health and Management Society Ecovision Series.Google Scholar

Copyright information

© Coastal and Estuarine Research Federation (outside the USA) 2012

Authors and Affiliations

  • Joel C. Hoffman
    • 1
    Email author
  • John R. Kelly
    • 1
  • Greg S. Peterson
    • 1
  • Anne M. Cotter
    • 1
  • Matthew A. Starry
    • 2
  • Michael E. Sierszen
    • 1
  1. 1.Mid-Continent Ecology Division, National Health and Environmental Effects Research LabUS EPA Office of Research and DevelopmentDuluthUSA
  2. 2.SRA International, IncDuluthUSA

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