, Volume 629, Issue 1, pp 147–156 | Cite as

Responses of benthic–pelagic coupling to climate change in a temperate estuary

  • Robinson W. FulweilerEmail author
  • Scott W. Nixon


This article reports the first demonstration of the impact of climate change on benthic–pelagic coupling and the biogeochemical cycles of a coastal marine system. Over the last 30 years Narragansett Bay, a 328-km2 temperate estuary on the east coast of the United States, has undergone a variety of ecological changes. Building on a robust data set that spans three decades, we present a link between warming (+1.7°C in annual mean water temperature) in the bay and a marked decrease in sediment oxygen consumption, in the fluxes of ammonium and phosphate from sediments to the overlying water, and in sediment denitrification. We attribute this reduction in biogeochemical exchange to a dramatic drop in the standing crop of water-column chlorophyll as the system has shifted from one characterized by a dominant winter–spring bloom to one supported by more ephemeral and less intense summer–autumn blooms. The recent climate-induced oligotrophication of the bay will be further exacerbated by forthcoming nitrogen reductions due to tertiary sewage treatment.


Climate change Benthic–pelagic coupling Oligotrophication Denitrification Nutrient regeneration Phenology 



We thank the organizing committee and sponsors for the International Symposium on Research and Management of Eutrophication in Coastal Ecosystems, where the material contained in this manuscript was first presented. We also thank B. Buckley for analyzing the most recent nutrient samples and S. Granger for his help in field core collection. Others who helped in core collection are: P. Dimilla, K. Hanks, M. Horn, J. Krumholz, C. Mueller, A. Pimenta, and M. Traber. Many thanks to A. Giblin and J. Tucker of the Ecosystems Center, Marine Biological Laboratory, Woods Hole, MA, for their help in denitrification analysis. J. Cornwell and M. Owens of the University of Maryland, Horn Point Laboratory helped with core design and construction, and sample analysis. The historic data were collected and/or analyzed by B. Nowicki, S. Hale, R. Chinman, and J. Kelly in collaboration with S. Nixon and C. Oviatt. R.W. Fulweiler was funded in part to complete this study by the Rhode Island Coastal Resources Management Council. The Graduate School of Oceanography Alumni Association and the Robert and Patricia Switzer Foundation provided travel support for R.W. Fulweiler to participate in the symposium.


  1. Beatty, L. L., 1991. The response of benthic suspension feeders and their grazing impact on phytoplankton in eutrophied coastal ecosystems. Ph.D. Thesis, University of Rhode Island, Graduate School of Oceanography, Narragansett, RI, 352 pp.Google Scholar
  2. Borkman, D. G., 2002. Analysis and simulation of Skeletonema costatum (Grev.) Cleve annual abundance patterns in lower Narragansett Bay 1959–1996. Ph.D. Thesis, University of Rhode Island, Graduate School of Oceanography, Narragansett, RI, 395 pp.Google Scholar
  3. Brush, M. J., J. W. Brawley, S. W. Nixon & J. N. Kremer, 2002. Modeling phytoplankton production: problems with the Eppley curve and an empirical alternative. Marine Ecological Progress Series 238: 31–45.CrossRefGoogle Scholar
  4. Carrit, D. E. & J. H. Carpenter, 1966. Recommendation procedure for Winkler analyses of sea water for dissolved oxygen. Journal of Marine Research 24: 313–318.Google Scholar
  5. Colt, J., 1984. Computation of dissolved gas concentrations in water as functions of temperature, salinity, and pressure. American Fisheries Society Special Publication 14.Google Scholar
  6. Craig, N. I., 1989. Age and growth history characteristics of Nucula annulata in undisturbed and nutrient enhanced environments. M.S. Thesis, University of Rhode Island, 93 pp.Google Scholar
  7. de Jonge, V. N., W. Boynton, C. F. D’Elia, R. Elmgren & B. L. Welsh, 1994. Responses to developments in eutrophication in four different North Atlantic estuarine systems. In Dyer, K. R. & R. J. Orth (eds), Changes in Fluxes in Estuaries. Olsen & Olsen, Fredensberg: 179–196.Google Scholar
  8. Doering, P. H., 1989. On the contribution of the benthos to pelagic production. Journal of Marine Research 47: 371–383.CrossRefGoogle Scholar
  9. Doering, P. H., C. A. Oviatt & J. R. Kelly, 1986. The effects of the filter-feeding clam Mercenaria mercenaria on carbon cycling in experimental marine mesocosms. Journal of Marine Research 44: 839–861.CrossRefGoogle Scholar
  10. Edwards, M. & A. J. Richardson, 2004. Impact of climate change in marine pelagic phenology and trophic mismatch. Nature 430: 881–884.PubMedCrossRefGoogle Scholar
  11. Ellis, G., 2002. An examination of the benthic macrofauna of Narragansett Bay and the possible implications of winter–spring bloom intensity on population size. M.S. Thesis, University of Rhode Island, Narragansett, RI.Google Scholar
  12. Emanuel, K. A., 2005. Increasing destructiveness of tropical cyclones over the past 30 years. Nature 436: 686–688.PubMedCrossRefGoogle Scholar
  13. Eyre, B. D., S. Rysgaard, T. Dalsgaard & P. B. Christensen, 2002. Comparison of isotope pairing and N2:Ar methods for measuring sediment denitrification—assumptions, modifications, and implications. Estuaries 25: 1077–1087.CrossRefGoogle Scholar
  14. Farnsworth, E. J., J. Núñez-Farfán, S. A. Careaga & F. A. Bazzaz, 1995. Phenology and growth of three temperate forest life forms in response to artificial soil warming. Journal of Ecology 83: 967–977.CrossRefGoogle Scholar
  15. Frithsen, J. B., 1989. The benthic communities within Narragansett Bay: an assessment completed for the Narragansett Bay Project. Rhode Island Department of Environmental Management, Providence, RI, 28 pp.Google Scholar
  16. Furnas, M. J., G. L. Hitchcock & T. J. Smayda, 1976. Nutrient-phytoplankton relationships in Narragansett Bay during the 1974 summer bloom. In Wiley, M. (ed.), Estuarine Processes: Uses, Stresses, and Adaptation to the Estuary, Vol. 1. Academic Press, New York: 118–133.Google Scholar
  17. Garber, J. H., 1982. 15N-tracer and other laboratory studies of nitrogen remineralization in sediments and waters from Narragansett Bay, Rhode Island. Ph.D. Thesis, University of Rhode Island, Graduate School of Oceanography, Narragansett, RI, 276 pp.Google Scholar
  18. Giblin, A., C. Hopkinson, J. Tucker, B. Nowicki & J. Kelly, 1995. Metabolism, nutrient cycling and denitrification in Boston harbor and Massachusetts Bay sediments in 1994. MWRA Environmental Quality Report Series No. 95-13. MA Water Resources Authority, Boston, 56 pp.Google Scholar
  19. Grall, J. & L. Chauvaud, 2002. Marine eutrophication and benthos: the need for new approaches and concepts. Global Change Biology 8: 813–830.CrossRefGoogle Scholar
  20. Grasshoff, K., 1976. Methods of Seawater Analysis, 2nd Edition. Verlag Chemie, Weinheim.Google Scholar
  21. Grassle, J. F., J. P. Grassle, L. S. Brown-Leger, R. F. Petrecca, N. J. Copley, 1985. Subtidal macrobenthos of Narragansett Bay. Field and mesocosm studies of the effects of eutrophication and organic input on benthic populations. In Gray, J. S. & M. E. Christiansen (eds), Marine Biology of Polar Regions and Effects of Stress on Marine Organisms. John Wiley, New York: 421–434.Google Scholar
  22. Groffman, P. M., M. Altabet, J. K. Bohlke, K. Butterbach-Bahl, M. B. David, M. K. Firestone, A. E. Giblin, T. M. Kana, L. P. Nielsen & M. A. Voytek, 2006. Methods for measuring denitrification: diverse approaches to a difficult problem. Ecological Applications 16: 2091–2122.PubMedCrossRefGoogle Scholar
  23. Hale, S., 1974. The role of benthic communities in the nutrient cycles of Narragansett Bay. Ph.D. Thesis, University of Rhode Island, Narragansett, RI.Google Scholar
  24. Hawk, J. D., 1998. The role of the North Atlantic oscillation in winter climate variability as it relates to the winter–spring bloom in Narragansett Bay. M.S. Thesis, University of Rhode Island, Narragansett, RI.Google Scholar
  25. Inouye, D. W., B. Barr, K. B. Armitage & B. D. Inouye, 2000. Climate change is affecting altitudinal migrants and hibernating species. Proceedings of the National Academy of Sciences 97: 1630–1633.CrossRefGoogle Scholar
  26. Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, R. H. Bradbury, R. Cooke, J. Erlandson, J. A. Estes, T. P. Hughes, S. Kidwell, C. B. Lange, H. S. Lenihan, J. M. Pandolfi, C. H. Peterson, R. S. Steneck, M. J. Tegner & R. R. Warner, 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293: 629–637.PubMedCrossRefGoogle Scholar
  27. Josefson, A. B. & B. Rasmussen, 2000. Nutrient retention by benthic macrofaunal biomass of Danish estuaries: importance of nutrient load and residence time. Estuarine, Coastal and Shelf Science 50: 205–216.CrossRefGoogle Scholar
  28. Kana, T. M., C. Darkangelo, M. D. Hunt, J. B. Oldham, E. Bennett & J. C. Cornwell, 1994. Membrane inlet mass-spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Analytical Chemistry 66: 4166–4170.CrossRefGoogle Scholar
  29. Karentz, D. & T. J. Smayda, 1998. Temporal patterns of variations in phytoplankton community organization and abundance in Narragansett Bay during 1959–1980. Journal of Plankton Research 20: 145–168.CrossRefGoogle Scholar
  30. Keller, A. A. & U. Riebesell, 1989. Phytoplankton carbon dynamics during a winter–spring diatom bloom in an enclosed marine ecosystem: primary production, biomass, and loss rates. Marine Biology 103: 131–142.CrossRefGoogle Scholar
  31. Keller, A. A., C. A. Ovaitt, H. A. Walker & J. D. Hawk, 1999. Predicted impacts of elevated temperature on the magnitude of the winter–spring phytoplankton bloom in temperate coastal waters: a mesocosm study. Limnology and Oceanography 44: 344–356.Google Scholar
  32. Kelly, J. R. & S. W. Nixon, 1984. Experimental studies of the effect of organic deposition on the metabolism of a coastal marine bottom community. Marine Ecology Progress Series 17: 157–169.CrossRefGoogle Scholar
  33. Kinney, E. H. & C. T. Roman, 1998. Response of primary producers to nutrient enrichment in a shallow estuary. Marine Ecological Progress Series 163: 89–98.CrossRefGoogle Scholar
  34. Kot-Wasik, A., J. Dębska & J. Namieśnik, 2004. Monitoring or organic pollutants in coastal waters of the Gulf of Gdansk, Southern Baltic. Marine Pollution Bulletin 49: 264–276.PubMedCrossRefGoogle Scholar
  35. Lambert, C. E. & C. A. Oviatt, 1983. Manual of Biological and Geochemical Techniques in Coastal Areas. MERL Publication Series, Report No. 1, 281 pp.Google Scholar
  36. Li, Y. & T. J. Smayda, 1998. Temporal variability of chlorophyll in Narragansett Bay 1973–1990. ICES Journal of Marine Science 55: 661–667.CrossRefGoogle Scholar
  37. McKenna, J. E., 1987. An analysis of food limitation in the benthic communities of Narragansett Bay using a numerical simulation model. Ph.D. Thesis, University of Rhode Island, Graduate School of Oceanography, Narragansett, RI, 293 pp.Google Scholar
  38. McMaster, R. L., 1960. Sediments of Narragansett Bay system and Rhode Island Sound, Rhode Island. Journal of Sedimentary Petrology 30: 249–274.Google Scholar
  39. Nixon, S. W., C. A. Oviatt & S. S. Hale, 1976. Nitrogen regeneration and the metabolism of coastal marine bottom communities. In Anderson, J. M. & A Macfayden (eds), The Role of Terrestrial and Aquatic Organisms in Decomposition Processes. Blackwell, Oxford: 269–283.Google Scholar
  40. Nixon, S. W., J. R. Kelly, B. N. Furnas, C. A. Oviatt & S. S. Hale, 1980. Phosphorus regeneration and the metabolism of coastal marine bottom communities. In Tenore, K. R. & B. C. Coull (eds), Marine Benthic Dynamics. University of South Carolina Press, Columbia: 219–242.Google Scholar
  41. Nixon, S. W., C. A. Oviatt, J. Frithsen & B. Sullivan, 1986. Nutrients and the productivity of estuarine and coastal marine ecosystems. Journal of the Limnological Society of Southern Africa 12: 43–71.Google Scholar
  42. Nixon, S. W., S. L. Granger & B. L. Nowicki, 1995. An assessment of the annual mass balance of carbon, nitrogen, and phosphorus in Narragansett Bay. Biogeochemistry 31: 15–61.CrossRefGoogle Scholar
  43. Nixon, S. W., S. Granger & B. Buckley, 2003. The warming of Narragansett Bay. 41ºN A Publication of Rhode Island Sea Grant and Land Grant Programs 2: 18–20. Available at:
  44. Nixon, S. W., S. Granger, B. A. Buckley, M. Lamont & B. Rowell, 2004. A one hundred and seventeen year coastal water temperature record from Woods Hole, Massachusetts. Estuaries 27: 397–404.CrossRefGoogle Scholar
  45. Nixon, S. W., B. Buckley, S. Granger, L. Harris, A. Oczkowski, L. Cole & R. Fulweiler, 2005. Anthropogenic nutrients to Narragansett Bay: a twenty-five year perspective. A Report to the Narragansett Bay Commission and Rhode Island Sea Grant. Available at
  46. Nixon, S. W., B. Buckley, S. Granger, L. Harris, A. Oczkowski, R. Fulweiler & L. Cole, 2008. Nutrient inputs to Narragansett Bay: past, present, and future. In Desbonnet, A., A. B. Colt & B. A. Costa-Pierce (eds), Science of Ecosystem-Based Estuary Management: Narragansett Bay in the 21st Century. Springer, New York: 101–175.Google Scholar
  47. Nowicki, B. L., 1994. The effect of temperature, oxygen, salinity, and nutrient enrichment on estuarine denitrification rates measured with a modified nitrogen gas flux technique. Estuarine, Coastal and Shelf Science 38: 137–156.CrossRefGoogle Scholar
  48. Nowicki, B. L. & C. A. Oviatt, 1990. Are estuaries traps for anthropogenic nutrients? Evidence from estuarine mesocosms. Marine Ecology Progress Series 66: 131–146.CrossRefGoogle Scholar
  49. O’Reilly, J. E., 1984. Carbon flow in a coastal marine bottom community. Ph.D. Thesis, University of Rhode Island, 199 pp.Google Scholar
  50. Oviatt, C. A., 2004. The changing ecology of temperate coastal waters during a warming trend. Estuaries 27: 895–904.CrossRefGoogle Scholar
  51. Oviatt, C. A., P. Doering, B. L. Nowicki & A. Zoppini, 1993. Net system production in coastal waters as a function of eutrophication, seasonality, and benthic macrofaunal abundance. Estuaries 16: 247–254.CrossRefGoogle Scholar
  52. Oviatt, C. A., P. Doering, B. Nowicki, L. Reed, J. Cole & J. Frithsen, 1995. An ecosystem level experiment on nutrient limitation in temperate coastal marine environments. Marine Ecology Progress Series 116: 171–179.CrossRefGoogle Scholar
  53. Oviatt, C., A. Keller & L. Reed, 2002. Annual primary production in Narragansett Bay with no bay-wide winter–spring phytoplankton bloom. Estuarine, Coastal and Shelf Science 54: 1013–1026.CrossRefGoogle Scholar
  54. Pilson, M. E. Q., 1985. On the residence time of water in Narragansett Bay. Estuaries 8: 2–14.CrossRefGoogle Scholar
  55. Pratt, D. M., 1959. The phytoplankton of Narragansett Bay. Limnology and Oceanography 4: 425–440.CrossRefGoogle Scholar
  56. Rhode Island Department of Environmental Management, 2003. The Greenwich Bay Fish Kill—August 2003. Causes, Impacts and Responses Report. 32 pp.Google Scholar
  57. Rudnick, D. T. & C. A. Oviatt, 1986. Seasonal lags between organic carbon deposition and mineralization in marine sediments. Journal of Marine Research 44: 815–837.CrossRefGoogle Scholar
  58. Rudnick, D. T., R. Elmgren & J. B. Frithsen, 1985. Meiofaunal prominence and benthic seasonality in a coastal marine ecosystem. Oecologia 67: 157–168.CrossRefGoogle Scholar
  59. Scavia, D., J. C. Field, D. F. Boesch, R. W. Buddemeier, V. Burkett, D. R. Cayan, M. Fogarty, M. A. Harwell, R. W. Howarth, C. Mason, D. J. Reed, T. C. Royer, A. H. Sallenger & J. G. Titus, 2002. Climate change impacts on U.S. Coastal and Marine Ecosystems. Estuaries 25: 149–164.CrossRefGoogle Scholar
  60. Seitzinger, S., S. W. Nixon & M. E. Q. Pilson, 1984. Denitrification and nitrous oxide production in a coastal marine ecosystem. Limnology and Oceanography 29: 73–83.Google Scholar
  61. Sullivan, B. K., D. VanKeuren & M. Clancy, 2001. Timing and size of blooms of the ctenophore Mnemiopsis leidyi in relation to temperature in Narragansett Bay, Rhode Island. Hydrobiologia 451: 113–120.CrossRefGoogle Scholar
  62. Townsend, D. W. & L. M. Cammen, 1988. Potential importance of the timing of spring plankton blooms to benthic–pelagic coupling and recruitment of juvenile demersal fishes. Biological Oceanography 5: 215–229.Google Scholar
  63. US EPA, 1983a. Methods for chemical analysis of water and wastes, EPA-600/4-79-020, Revised March 1983, Method 365.3. U.S. Environmental Protection Agency, Ohio.Google Scholar
  64. US EPA, 1983b. Methods for chemical analysis of water and wastes. EPA-600/4-79-020, Revised March 1983, Method 365.5. U.S. Environmental Protection Agency, Ohio.Google Scholar
  65. US EPA, 1997. Determination of nitrate and nitrite in estuarine and coastal waters by gas segmented continuous flow colorimetric analysis. In Ortner, P. B. & C. J. Fischer (eds), Methods for Chemical Analysis of Water and Wastes, Revision 2.0, Method 353.4. U.S. Environmental Protection Agency, Ohio.Google Scholar
  66. Valiela, I., K. Foreman, M. LaMontagne, D. Hersh, J. Costa, P. Peckol, B. DeMeo-Anderson, C. D’Avanzo, M. Babione, C. Sham, J. Brawley & K. Lajtha, 1992. Couplings of watersheds and coastal waters: sources and consequences of nutrient enrichment in Waquoit Bay, Massachusetts. Estuaries 15: 443–457.CrossRefGoogle Scholar
  67. Walther, G., E. Post, P. Convey, A. Menzel, C. Parmesan, J. C. Beebee, J. Fromentin, O. Hoegh-Guldberg & F. Bairlein, 2002. Ecological response to recent climate change. Nature 416: 389–395.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Department of Earth SciencesBoston UniversityBostonUSA
  2. 2.Graduate School of OceanographyUniversity of Rhode IslandNarragansettUSA

Personalised recommendations