Abstract
Narragansett Bay has been heavily influenced by human activities for more than 200 years. In recent decades, it has been one of the more intensively fertilized estuaries in the USA, with most of the anthropogenic nutrient load originating from sewage treatment plants (STP). This will soon change as tertiary treatment upgrades reduce nitrogen (N) loads by about one third or more during the summer. Before these reductions take place, we sought to characterize the sewage N signature in primary (macroalgae) and secondary (the hard clam, Mercenaria mercenaria) producers in the bay using stable isotopes of N (δ15N) and carbon (δ13C). The δ15N signatures of the macroalgae show a clear gradient of approximately 4‰ from north to south, i.e., high to low point source loading. There is also evidence of a west to east gradient of heavy to light values of δ15N in the bay consistent with circulation patterns and residual flows. The Providence River Estuary, just north of Narragansett Bay proper, receives 85% of STP inputs to Narragansett Bay, and lower δ15N values in macroalgae there reflected preferential uptake of 14N in this heavily fertilized area. Differences in pH from N stimulated photosynthesis and related shifts in predominance of dissolved C species may control the observed δ13C signatures. Unlike the macroalgae, the clams were remarkably uniform in both δ15N (13.2 ± 0.54‰ SD) and δ13C (−16.76 ± 0.61‰ SD) throughout the bay, and the δ15N values were 2–5‰ heavier than in clams collected outside the bay. We suggest that this remarkable uniformity reflects a food source of anthropogenically heavy phytoplankton formed in the upper bay and supported by sewage derived N. We estimate that approximately half of the N in the clams throughout Narragansett Bay may be from anthropogenic sources.
Similar content being viewed by others
References
Beatty, L.L. 1991. The response of benthic suspension feeders and their grazing impact on phytoplankton in eutrophied coastal ecosystems. Ph.D. Dissertation, University of Rhode Island, Narragansett, Rhode Island.
Bergondo, D.L. 2004. Examining the processes controlling water column variability in Narragansett Bay: Time series data and numerical modeling. Ph.D. Dissertation, University of Rhode Island, Narragansett, Rhode Island.
Bergondo, D.L., D.R. Kester, H.E. Stoffel, and W.L. Woods. 2005. Time-series observations during the low sub-surface oxygen events in Narragansett Bay during summer 2001. Marine Chemistry 97: 90–103.
Bricelj, V., A. Bass, and G. Lopez. 1984. Absorption and gut passage time of microalgae in a suspension feeder: An evaluation of the 51Cr:14C twin tracer technique. Marine Ecology Progress Series 17: 57–63.
Campbell, R.G. 1993. Studies of feeding behavior, development, and food limitation in first feeding nauplii of the copepod Acartia tonsa (Copepoda: Calanoida). Ph.D. Dissertation, University of Rhode Island, Narragansett, Rhode Island.
Carmichael, R.H. 2004. The effects of eutrophication on Mya arenaria and Mercenaria mercenaria: Growth, survival, and physiological responses to changes in food supply and habitat across estuaries receiving different N loads. Ph.D. Dissertation, Boston University, Boston, Massachusetts.
Cassar, N., E. Laws, R. Bidigare, and B. Popp. 2004. Bicarbonate uptake by Southern Ocean phytoplankton. Global Biogeochemical Cycles 18: DOI 10.1029/2003GB002116.
Chanton, J.P., and F.G. Lewis. 1999. Plankton and dissolved inorganic carbon composition in a river-dominated estuary: Apalachicola Bay, Florida. Estuaries 22: 575–583.
Chaves, J.E. 2004. Potential use of 15N to assess nitrogen sources and fate in Narragansett Bay. Ph.D. Dissertation, University of Rhode Island, Narragansett, Rhode Island.
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: 102–115.
Cole, M.L., I. Valiela, K.D. Kroeger, G.L. Tomasky, J. Cebrian, C. Wigand, R.A. McKinney, S.P. Grady, and M.H.C. da Silva. 2004. Assessment of a δ15N isotopic method to indicate anthropogenic eutrophication in aquatic ecosystems. Journal of Environmental Quality 33: 124–132.
Cole, M.L., K.D. Kroeger, J.W. McClelland, and I. Valiela. 2006. Effects of watershed land use on nitrogen concentrations and δ15 nitrogen in groundwater. Biogeochemistry 77: 199–215.
Cook, C., T. Lanaras, and B. Colman. 1986. Evidence for bicarbonate transport in species of red and brown macrophytic marine algae. Journal of Experimental Botany 37: 977–984.
Cornelisen, C.D., S.R. Wing, K.L. Clark, M.H. Bowman, R.D. Frew, and C.L. Hurd. 2007. Patterns in the δ13C and δ15N signature of Ulva pertusa: Interaction between physical gradients and nutrient source pools. Limnology and Oceanography 52: 820–832.
Costanzo, S.D., M.J. O’Donohue, W.C. Dennison, N.R. Loneragan, and M. Thomas. 2001. A new approach for detecting and mapping sewage impacts. Marine Pollution Bulletin 42: 149–156.
Culver-Rymsza, K. 1988. Occurrence of nitrate reductase along a transect of Narragansett Bay. M.S. Thesis, University of Rhode Island, Narragansett, Rhode Island.
DiMilla, P. 2006. Using stable nitrogen isotopes to characterize and evaluate nitrogen sources to Greenwich Bay, RI and their influence on isotopic signatures in estuarine organisms. M.S. Thesis, University of Rhode Island, Narragansett, Rhode Island.
Doering, P., L. Weber, W. Warren, G. Hoffman, K. Schweitzer, M. Pilson, C. Oviatt, J. Cullen, and C. Brown. 1988. Monitoring of the Providence and Seekonk Rivers for trace metals and associated parameters, Data Report for SPRAY Cruises, 2 Volume. Marine Ecosystems Research Laboratory, University of Rhode Island, Narragansett, Rhode Island.
Doering, P.H., C.A. Oviatt, and M.E.Q. Pilson. 1990. Control of nutrient concentrations in the Seekonk–Providence River region of Narragansett Bay, Rhode Island. Estuaries 13: 418–430.
Drechsler, Z., R. Sharkia, Z. Cabantchik, and S. Beer. 1993. Bicarbonate uptake in the marine macroalgae Ulva sp. is inhibited by classical probes of anion exchange by red blood cells. Planta 191: 34–40.
Durbin, A.G., and E.G. Durbin. 1981. Standing stock and estimated production rates of phytoplankton and zooplankton in Narragansett Bay, R.I. Estuaries 4: 24–41.
Fry, B. 2002. Conservative mixing of stable isotopes across estuarine salinity gradients: A conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25: 264–271.
Fry, B. 2006. Stable isotope ecology. New York: Springer.
Fry, B., and E. Sherr. 1984. 13C Measurements as indicators of carbon flow in marine and freshwater ecosystems. Contributions in Marine Science, University of Texas 27: 13–47.
Fry, B., and S.C. Wainright. 1991. Diatom sources of δ13C-rich carbon in marine food webs. Marine Ecology Progress Series 76: 149–157.
Galloway, J.N., and E.B. Cowling. 2002. Reactive nitrogen and the world: 200 years of change. Ambio 31: 64–71.
Garber, J.H. 1982. 15N-tracer and other laboratory studies of nitrogen remineralization in sediments and waters from Narragansett Bay, Rhode Island. Ph.D. Dissertation, University of Rhode Island, Narragansett, Rhode Island.
Gearing, J.N., P.J. Gearing, D.T. Rudnick, A.G. Requejo, and M.J. Hutchins. 1984. Isotopic variability of organic carbon in a phytoplankton-based, temperate estuary. Geochimica et Cosmochimica Acta 48: 1089–1098.
Gearing, P.J., J.N. Gearing, J.T. Maughan, and C.A. Oviatt. 1991. Isotopic distribution of carbon from sewage sludge and eutrophication in the sediments and food web of estuarine ecosystems. Environmental Science and Technology 25: 295–301.
Grassle, J.P., and J.F. Grassle. 1984. The utility of studying the effects of pollutants on single species populations in benthos of mesocosms and coastal ecosystems. In Concepts in Marine Pollution Measurements, ed. H. White, , 621–642. Maryland: Maryland Sea Grant College Park, College Park.
Hess, K.W., and F.M. White. 1974. A numerical tidal model of Narragansett Bay. University of Rhode Island Marine Technical Report Number 20. Rhode Island Sea Grant, Narragansett, Rhode Island.
Hobbie, J.E., U. Larsson, R. Elmgren, and B. Fry. 1990. Sewage derived 15N in the Baltic traced in Fucus. Eos 71: 190.
Hunt, C., M. Fox, S. Jackson, and M. Pilson. 1987. Narragansett Bay water quality monitoring and source strength measurements. Cruise and Data Report for SINBADD 4. Marine Ecosystems Research Laboratory, University of Rhode Island, Narragansett, Rhode Island.
Iverson, R.L. 1990. Control of marine fish production. Limnology and Oceanography 35: 1593–1604.
JMP Release 6.0.0. 2005. JMP User Guide, Release 6. SAS, Inc., Cary, North Carolina.
Jones, D.S., M.A. Arthur, and D.J. Allard. 1989. Sclerochronological records of temperature and growth from shells of Mercenaria mercenaria from Narragansett Bay, Rhode Island. Marine Biology 102: 225–234.
Keller, A., J. Frithsen, C. Oviatt, J. Maughan, B. Sullivan, S. Nixon, and M. Pilson. 1987. Marine ecosystem responses to sewage sludge and inorganic nutrient additions: A mesocosm experiment data report. MERL Series, Report No. 6, University of Rhode Island, Narragansett, Rhode Island.
Keller, A.A., P.H. Doering, S.P. Kelly, and B.K. Sullivan. 1990. Growth of juvenile Atlantic menhaden Brevoortia tyrannus (Pisces: Clupeidae) in MERL mesocosms: Effects of eutrophication. Limnology and Oceanography 35: 109–122.
Keller, A., C. Oviatt, H. Walker, and J. Hawk. 1999. Predicted impacts of elevated temperature on the magnitude of the winter–spring phytoplankton bloom in temperate coastal waters. Limnology and Oceanography 44: 344–356.
Kemp, W.M., W.R. Boynton, J.E. Adolf, D.F. Boesch, W.C. Boicourt, G. Brush, J.C. Cornwell, T.R. Fisher, P.M. Glibert, J.D. Hagy, L.W. Harding, E.D. Houde, D.G. Kimmel, W.D. Miller, R.I.E. Newell, M.R. Roman, E.M. Smith, and J.C. Stevenson. 2005. Eutrophication of Chesapeake Bay: Historical trends and ecological interactions. Marine Ecology Progress Series 303: 1–29.
Kincaid, C. 2006. The exchange of water through multiple entrances to the Mount Hope Estuary. Northeast Naturalist 13: 117–144.
Kincaid, K., D. Bergondo, and K. Rosenberger. 2008. Circulation and exchange between lower Narragansett Bay and Rhode Island Sound. In Science for Ecosystem-Based Management: Narragansett Bay in the 21st Century, eds. B. Costa-Pierce, , and A. Desbonet, , 301–324. New York: Springer.
Kincaid, C., R. Pockalny, and L. Huzzey. 2003. Spatial and temporal variability in flow at the mouth of Narragansett Bay. Journal of Geophysical Research 108:11–1 to 11–18.
Kremer, J.N., and S.W. Nixon. 1978. A coastal marine ecosystem, simulation and analysis. New York: Springer.
Larsson, C., and L. Axelsson. 1999. Bicarbonate uptake and utilization in marine macroalgae. European Journal of Phycology 34: 79–86.
Larsson, C., L. Axelsson, H. Ryberg, and S. Beer. 1997. Photosynthetic carbon utilization by Enteromorpha intestinalis (Chlorophyta) from a Swedish rockpool. European Journal of Phycology 32: 49–54.
Lee, V., and S. Olsen. 1985. Eutrophication and management initiatives for the control of nutrient inputs to Rhode Island coastal lagoons. Estuaries 8: 191–202.
Loosanoff, V. 1939. Effect of temperature upon shell movements of clams, Venus mercenaria (L.). Biological Bulletin 76: 171–182.
Maberly, S.C. 1990. Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. Journal of Phycology 26: 439–449.
Maberly, S.C., J.A. Raven, and A.M. Johnston. 1992. Discrimination between 12C and 13C by marine plants. Oecologia 91: 481–492.
Marine Research Inc. 1976. Charlestown Site Study Annual Report, April 1975–March 1976, Appendix Volume 6. Falmouth, Massachusetts: Marine Research Inc.
Mariotti, A. 1983. Atmospheric nitrogen is a reliable standard for natural 15N abundance measurements. Nature 303: 685–687.
Martinetto, P., M. Teichberg, and I. Valiela. 2006. Coupling of estuarine benthic and pelagic food webs to land-derived nitrogen sources in Waquoit Bay, Massachusetts, USA. Marine Ecology Progress Series 307: 37–48.
Maughan, J.T. 1986. Relationship between macrobenthic infauna and organic carbon. Ph.D. Dissertation, University of Rhode Island, Narragansett, Rhode Island.
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.
Menéndez, M., M. Martínez, and F.A. Comín. 2001. A comparative study of the effect of pH and inorganic carbon resources on the photosynthesis of three floating macroalgae species of a Mediterranean coastal lagoon. Journal of Experimental Marine Biology and Ecology 256: 123–136.
Nixon, S.W. 1988. Physical energy inputs and the comparative ecology of lake and marine ecosystems. Limnology and Oceanography 33: 1005–1025.
Nixon, S.W., and B.A. Buckley. 2002. “A strikingly rich zone”—Nutrient enrichment and secondary production in coastal marine ecosystems. Estuaries 25: 782–796.
Nixon, S.W., and M.E. Pilson. 1983. Nitrogen in estuarine and coastal marine ecosystems. In Nitrogen in the marine environment, eds. E. J. Carpenter, , and D. G. Capone, , 565–648. New York: Academic Press.
Nixon, S., B. Furnas, R. Chinman, and S. Heffernan. 1982. Nutrient inputs to Rhode Island coastal lagoons and salt ponds. Report to RI Statewide Planning, University of Rhode Island, Narragansett, Rhode Island.
Nixon, S.W., S.L. Granger, and B.L. Nowicki. 1995. An assessment of the annual mass balance of carbon, nitrogen, and phosphorous in Narragansett Bay. Biogeochemistry 31: 15–61.
Nixon, S., B. Buckley, S. Granger, L. Harris, A. Oczkowski, L. Cole, and R. Fulweiler. 2005. Anthropogenic inputs to Narragansett Bay, a twenty-five year perspective. Report to the Narragansett Bay Commission and Rhode Island Sea Grant, Narragansett, RI. http://seagrant.gso.uri.edu/research/bay_commission_report.pdf.
Nixon, S.W., B. Buckley, S. Granger, L.A. Harris, A.J. Oczkowski, R.W. Fulweiler, and L.W. Cole. 2008. Nutrient (N and P) inputs to Narragansett Bay: Past, present, and future. In Ecosystem Based Management: A Case Study of Narragansett Bay. Springer Series in Environmental Management, eds. A. Desbonnet, , and B. A. Costa-Pierce, , 101–176. New York: Springer.
Nowicki, B., and A.J. Gold. 2008. Nutrient transport in groundwater at the coastal margin. In Ecosystem Based Management: A Case Study of Narragansett Bay. Springer Series in Environmental Management, eds. A. Desbonnet, , and B. A. Costa-Pierce, , 67–100. New York: Springer.
Oviatt, C., P. Doering, B. Nowicki, L. Reed, J. Cole, and J. Frithsen. 1995. An ecosystem level experiment on nutrient limitation in temperate coastal marine environments. Marine Ecology Progress Series 116: 171–179.
Oviatt, C., A. Keller, and 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.
Pilson, M.E.Q. 1985a. Annual cycles of nutrients and chlorophyll in Narragansett Bay, Rhode Island. Journal of Marine Research 43: 849–873.
Pilson, M.E.Q. 1985b. On the residence time of water in Narragansett Bay. Estuaries 8: 2–14.
Pilson, M.E.Q. 1998. An Introduction to the Chemistry of the Sea. New Jersey: Prentice Hall, Upper Saddle River.
Pilson, M.E.Q. 2008. Narragansett Bay amidst a globally changing climate. In Ecosystem Based Management: A Case Study of Narragansett Bay. Springer Series in Environmental Management, eds. A. Desbonnet, , and B. A. Costa-Pierce, , 35–46. New York: Springer.
Pratt, D.M. 1959. The winter–spring diatom flowering in Narragansett Bay. Limnology and Oceanography 10: 173–184.
Pratt, D.M., and D.A. Campbell. 1956. Environmental factors affecting growth in Venus mercenaria. Limnology and Oceanography 7: 2–17.
Pruell, R.J., B.K. Taplin, J.L. Lake, and S. Jayaraman. 2006. Nitrogen isotope ratios in estuarine biota collected along a nutrient gradient in Narragansett Bay, Rhode Island, USA. Marine Pollution Bulletin 52: 612–620.
Rau, G.H., R.E. Sweeney, I.R. Kaplan, A.J. Mearns, and D.R. Young. 1981. Differences in animal 13C, 15N and D abundance between polluted and an unpolluted coastal site: Likely indicators of sewage uptake by a marine food web. Estuarine Coastal and Shelf Science 13: 701–707.
Raven, J.A. 1997. Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research 27: 85–209.
Raven, J.A., A.M. Johnston, J.E. Kübler, R. Korb, S.G. McInroy, L.L. Handley, C.M. Scrimgeour, D.I. Walker, J. Beardall, M. Vanderklift, S. Fredriksen, and K.H. Dunton. 2002. Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Functional Plant Biology 29: 355–378.
Rudnick, D.T., R. Elmgren, and J.B. Frithsen. 1985. Meiofaunal prominence and benthic seasonality in a coastal marine ecosystem. Oecologia 67: 157–168.
Sand-Jensen, K., and D. Gordon. 1984. Differential ability of marine and freshwater macrophytes to utilize \({\text{HCO}}_3^ - \) and CO2. Marine Biology 80: 247–253.
SAS Institute, Inc. 1982. SAS User’s Guide Basics. Cary, North Carolina: SAS, Inc..
Savage, C., and R. Elmgren. 2004. Macroalgal (Fucus vesiculosus) δ15N values trace decrease in sewage effluent. Ecological Applications 14: 517–526.
Schell, D.M. 2000. Declining carrying capacity in the Bering Sea: Isotopic evidence from whale baleen. Limnology and Oceanography 45: 459–462.
Seitzinger, S.P., R.V. Styles, E.W. Boyer, R.B. Alexander, G. Billen, R.W. Howarth, B. Mayer, and N. Van Breemen. 2002. Nitrogen retention in rivers: Model development and application to watersheds in the northeastern U.S.A. Biogeochemistry 57/58: 199–237.
Sheats, N. 2000. The use of stable isotopes to define the extent of incorporation of sewage nitrogen into aquatic food webs and to discern differences in habitat suitability within a single estuary. Ph.D. Dissertation, Harvard University, Cambridge, Massachusetts.
Smith, S.V., and P. Kroopnick. 1981. Carbon-13 isotopic fractionation as a measure of aquatic metabolism. Nature 294: 252–253.
Spies, R.B., H.P. Kruger, R. Ireland, and D.W. Rice. 1989. Stable isotope ratios and contaminant concentrations in a sewage-distorted food web. Marine Ecology Progress Series 59: 33–38.
Sullivan, B.K., and P.J. Ritacco. 1985. Ammonia toxicity to larval copepods in eutrophic marine ecosystems: A comparison of results from bioassays and enclosed experimental ecosystems. Aquatic Toxicology 7: 205–217.
Thornber, C.S., DiMilla, P., Nixon, S., and McKinney, R. Uptake of nitrogen from natural and anthropogenic sources in bloom-forming macroalgae. Marine Pollution Bulletin. In Press.
Tucker, J., N. Sheats, A.E. Giblin, C.S. Hopkinson, and J.P. Montoya. 1999. Using stable isotopes to trace sewage-derived material through Boston Harbor and Massachusetts Bay. Marine Environmental Research 48: 353–375.
Valente, R.M., D.C. Rhoads, J.D. Germano, and V.J. Cabelli. 1992. Mapping of benthic enrichment patterns in Narragansett Bay, Rhode Island. Estuaries 15: 1–17.
Van Breemen, N., E.W. Boyer, C.L. Goodale, N.A. Jaworski, K. Paustian, S.P. Seitzinger, K. Lajtha, B. Mayer, D. Van Dam, R.W. Howarth, K.J. Nadelhoffer, M. Eve, and G. Billen. 2002. Where did all the nitrogen go? Fate of nitrogen inputs to large watersheds in the northeastern U.S.A. Biogeochemistry 57/58: 267–293.
Wozniak, A.S., C.T. Roman, S.C. Wainright, R.A. McKinney, and M.J. James-Pirri. 2006. Monitoring food web changes in tide-restored salt marshes: A carbon stable isotope approach. Estuaries and Coasts 29: 568–578.
York, J., G. Tomasky, and I. Valiela. 2007. Stable isotopic detection of ammonium and nitrate assimilation by phytoplankton in the Waquoit Bay estuarine system. Limnology and Oceanography 52: 144–155.
Zhang, J., P.D. Quay, and D.O. Wilbur. 1995. Carbon isotope fractionation during gas–water exchange and dissolution of CO2. Geochimica et Cosmochimica Acta 59: 107–114.
Acknowledgments
We would like to thank Jillian Hesse, Adam Pimenta, Amy Van Keuren, Jason Krumholtz, Matt Horn, and Amie Parris for their assistance in the laboratory and field, Boze Hancock from the National Oceanic and Atmospheric Administration (NOAA), Dennis Erkan the Rhode Island Department of Environmental Management, Division of Marine Fisheries for help with clam collection, and Jim Heltshe from the University of Rhode Island and the Environmental Protection Agency for assistance with statistical analyses. We would also like to thank the two anonymous reviewers of this manuscript for their insightful comments. This work was partially supported by Rhode Island Sea Grant, NOAA’s Dr. Nancy Foster Scholarship Program for A. Oczkowski, and The Nature Conservancy (TNC) through a scholarship to K. M. Henry. Additional support was provided by the Rhode Island Coastal Resources Management Program (NOAA). The statements, findings, conclusions, and recommendations are those of the authors and do not necessarily reflect the views of NOAA, TNC, or the Department of Commerce.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Oczkowski, A., Nixon, S., Henry, K. et al. Distribution and Trophic Importance of Anthropogenic Nitrogen in Narragansett Bay: An Assessment Using Stable Isotopes. Estuaries and Coasts: J CERF 31, 53–69 (2008). https://doi.org/10.1007/s12237-007-9029-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12237-007-9029-0