Over the past decade, nitrogen (N) loads to Narragansett Bay have decreased by more than 50%. These reductions were, in large part, the direct result of multiple wastewater treatment facility upgrades to tertiary treatment, a process which employs N removal. Here, we document ecosystem response to the N reductions and assess how the distribution of sewage N in Narragansett Bay has changed from before, during, and shortly after the upgrades. While others have observed clear responses when data were considered annually, our seasonal and regional comparisons of pre- and post-tertiary treatment dissolved inorganic nitrogen (DIN) concentrations and Secchi depth data, from bay-wide surveys conducted periodically from the early 1970s through 2016, resulted in only a few subtle differences. Thus, we sought to use stable isotope data to assess how sewage N is incorporated into the ecology of the Bay and how its distribution may have changed after the upgrades. The nitrogen (δ15N) and carbon (δ13C) stable isotope measurements of particulate matter served as a proxy for phytoplankton, while macroalgae served as short-term integrators of water column bio-available N, and hard clams (Mercenaria mercenaria) as integrators of water column production. In contrast to other estuarine stable isotope studies that have observed an increased influence of isotopically lower marine N when sewage N is reduced, the opposite has occurred in Narragansett Bay. The tertiary treatment upgrades have increased the effluent δ15N values by at least 2‰. The plants and animals throughout Narragansett Bay have similarly increased by 1–2‰, on average. In contrast, the δ13C values measured in particulate matter and hard clams have declined by about the same amount. The δ15N results indicated that, even after the N reductions, sewage N still plays an important role in supporting primary and secondary production throughout the bay. However, the δ13C suggests that overall net production in Narragansett Bay has decreased. In the 5 years after the major wastewater treatment facilities came on-line for nutrient removal, oligotrophication has begun but sewage remains the dominant source of N to Narragansett Bay.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Boesch, D.F. 2002. Challenges and opportunities in reducing nutrient over-enrichment of coastal ecosystems. Estuaries 25 (4): 886–900.
Borkman, D.G., and T. Smayda. 2009. Multidecadal (1959–1997) changes in Skeletonema abundance and seasonal bloom patterns in Narragansett Bay, Rhode Island, USA. Journal of Sea Research 61 (1-2): 84–94.
Borkman, D.G., and T.J. Smayda. 2016. Coincident patters of waste water suspended solids reduction, water transparency increase, and chlorophyll decline in Narragansett Bay. Marine Pollution Bulletin 107 (1): 161–169.
Brandes, J.A., and A.H. Devol. 1997. Isotopic fractionation of oxygen and nitrogen in coastal marine sediments. Geochimica et Cosmochimica Acta 61 (9): 1793–1801.
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, Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island.
Cantwell, M.G., D.R. Katz, J.C. Sullivan, K. Ho, and R.M. Burgess. 2017. Temporal and spatial behavior of pharmaceuticals in Narragansett Bay, Rhode Island, United States. Environmental Toxicology and Chemistry 36 (7): 1846–1855.
Chaves, J. E. 2004. Potential use of 15N to assess nitrogen sources and fate in Narragansett Bay. Ph.D. Dissertation, Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island.
Costanzo, S.D., J. Udy, B. Longstaff, and A. Jones. 2005. Using nitrogen stable isotope ratios (δ15N) of macroalgae to determine the effectiveness of sewage upgrades: Changes in the extent of sewage plumes over four years in Moreton Bay, Australia. Marine Pollution Bulletin 51 (1-4): 212–217.
DiMilla, P.A., 2006. Using stable nitrogen isotopes to characterize and evaluate nitrogen sources to Greenwich Bay, RI and their influence on isotopic signatures in estuarine organisms. MS Thesis, University of Rhode Island, Kingston, RI.
DiMilla, P.A., S.W. Nixon, A.J. Oczkowski, M.A. Altabet, and R.A. McKinney. 2011. Some challenges of an “upside down” nitrogen budget– Science and management in Greenwich Bay, RI (USA). Marine Pollution Bulletin 62 (4): 672–680.
Duarte, C.M., D.J. Conley, J. Carstensen, and M. Sánchez-Camacho. 2009. Return to Neverland: Shifting baselines affect eutrophication restoration targets. Estuaries and Coasts 32 (1): 29–36.
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 (1): 24–41.
Fry, B. 2006. Stable isotope ecology. Springer science+business media, LLC, New York, New York.
Fulweiler, R.W. and E.M. Heiss. 2014. (Nearly) a decade of directly measured sediment N2 fluxes: What can Narragansett Bay tell us about the global ocean nitrogen budget? 27: 184–195.
Fulweiler, R.W., A.J. Oczkowski, K.M. Miller, C.A. Oviatt, and M.E.Q. Pilson. 2015. Whole truths vs. half truths— And a search for clarity in long-term water temperature records. Estuarine, Coastal, and Shelf Science 157: A1–A6.
Fulweiler, R.W., H.E. Emery, and T.J. Maguire. 2016. A workflow for reproducing mean benthic gas fluxes. Earth and Space Science 3 (8): 318–325.
Garber, J. H. 1982. 15N-Tracer and Other Laboratory Studies of Nitrogen Remineralization in Sediments and Waters from Narragansett Bay, Rhode Island. Dissertation, University of Rhode Island, Kingston, RI.
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 (2): 295–301.
Granger, J., D.M. Sigman, J.A. Needoba, and P.J. Harrison. 2004. Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton. Limnology and Oceanography. 49 (5): 1763–1773.
Granger, J., D.M. Sigman, M.M. Rohde, M.T. Maldonade, and P.D. Tortell. 2010. N and O isotope effects during nitrate assimilation by unicellular prokaryotic and eukaryotic plankton cultures. Geochimica et Cosmochimica Acta. 74 (3): 1030–1040.
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. Maryland Sea Grant College Park, College Park, Maryland.
Greening, H., and A. Janicki. 2006. Toward reversal of eutrophic conditions in a subtropical estuary: Water quality and seagrass response to nitrogen load reductions in Tampa Bay, Florida, USA. Environmental Management 38 (2): 163–178.
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 springer, ed. B. Costa-Pierce and A. Desbonet, 301–324. New York: Verlag.
Kremer, J.N., and S.W. Nixon. 1978. A coastal marine ecosystem, simulation and analysis. New York: Springer-Verlag.
Krumholz, J.S. 2012. Spatial and temporal patterns in nutrient standing stock and mass-balance in response to load reductions in a temperate estuary. Ph.D. Dissertation, University of Rhode Island.
Li, Y., and T.J. Smayda. 2001. A chlorophyll time series for Narragansett Bay: Assessment of the potential effect of tidal phase on measurement. Estuaries and Coasts 24: 328–336.
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 (1): 203–214.
Melrose, D.C., J.S. Krumholz, and M.C. McManus. 2014. Measuring changes in total phytoplankton-sized particle volume over time as a proxy for primary production and food availability in narragansett Bay, RI. Proceedings of the 34th Milford Aquaculture Seminar. Journal of Shellfish Research 33: 541–565.
Narragansett Bay Estuary Program (NBEP). 2017. State of Narragansett Bay and Its Watershed. Technical Report, Providence, RI. http://nbep.org/the-state-of-our-watershed/technicalreport/. Accessed 19 December 2017.
Nixon, S.W., B. Buckley, S. Granger, L. Harris, A. Oczkowski, R. Fulweiler, and L. Cole. 2008. Nutrient (N and P) inputs to Narragansett Bay: Past, present, and future. In Science for ecosystem-based management Narragansett Bay in the 21st century, ed. A. Desbonnet and B.A. Costa-Pierce, 101–176. New York: Springer.
Nixon, S.W., R.W. Fulweiler, B.A. Buckley, S.L. Granger, B.L. Nowicki, and K.M. Henry. 2009. The impact of changing climate on phenology, productivity, and benthic-pelagic coupling in Narragansett Bay. Estuarine, coastal, and shelf. Science 82: 1–18.
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 (1): 53–69.
Oczkowski, A.J., M.E.Q. Pilson, and S.W. Nixon. 2010. A marked gradient in δ13C values of clams Mercenaria mercenaria across a marine embayment may reflect variations in ecosystem metabolism. Marine Ecology Progress Series 414: 145–153.
Oczkowski, A., E. Markham, A. Hanson, and C. Wigand. 2014. Carbon stable isotopes as indicators of coastal eutrophication. Ecological Applications 24 (3): 457–466.
Oczkowski, A., C.S. Thornber, E.E. Markham, R. Rossi, A. Ziegler, and S. Rinehart. 2015. Testing sample stability using four storage methods and the macroalgae Ulva and Gracilaria. Limnology and Oceanography: Methods 13: 9–14.
Oczkowski, A., B. Taplin, R. Pruell, A. Pimenta, R. Johnson, and J. Grear. 2018. Carbon stable isotope values in plankton and mussels reflect changes in carbonate chemistry associated with nutrient enhanced net production. Frontiers in Marine Science 5 https://doi.org/10.3389/fmars.2018.00043.
Oviatt, C.A. 2004. The changing ecology of temperate coastal waters during a warming trend. Estuaries 27 (6): 895–904.
Oviatt, C.A. 2008. Impacts of nutrients on Narragansett Bay productivity: A gradient approach. In Science for ecosystem-based management: Narragansett Bay in the 21st century, ed. A. Desbonnet and B.A. Costa-Pierce, 523–544. New York: Springer.
Oviatt, C.A., and R. Pastore. 1980. Some aspects of water quality in and pollution sources to the Providence River. Report for region 1 EPA September 1979–September 1980. Contract #68–04-1002, 02203. Boston, MA: United States Environmental Protection Agency.
Oviatt, C.A., M.E.Q. Pilson, S.W. Nixon, J.B. Frithsen, D.T. Rudnick, J.R. Kelly, J.F. Grassle, and J.P. Grassle. 1984. Recovery of a polluted estuarine system: A mesocosm experiment. Marine Ecology Progress Series 16: 203–217.
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., A.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 (6): 1013–1026.
Oviatt, C., L. Smith, J. Krumholz, C. Coupland, H. Stoffel, A. Keller, M.C. McManus, and L. Reed. 2017. Managed nutrient reduction impacts on nutrient concentrations, water clarity, primary production, and hypoxia in a north temperate estuary. Estuarine, Coastal, and Shelf Science 199: 25–34.
Paul, D., G. Skrzypek, and I. Fórizs. 2007. Normalization of measured stable isotopic compositions to isotope reference scales – A review. Rapid Communications in Mass Spectrometry 21 (18): 3006–3014.
Pedersen, M.F., and J. Borum. 1996. Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Marine Ecology Progress Series 142: 261–272.
Perez, K.T., E.W. Davey, R.H. Moore, P.R. Burn, M.S. Rosol, J.A. Cardin, R.L. Johnson, and D.N. Kopans. 1999. Application of computer-aided tomography (CT) to the study of estuarine benthic communities. Ecological Applications 9 (3): 1050–1058.
Pilson, M.E.Q. 1985a. Annual cycles of nutrients and chlorophyll in Narragansett Bay, Rhode Island. Journal of Marine Research 43 (4): 849–873.
Pilson, M.E.Q. 1985b. On the residence time of water in Narragansett Bay. Estuaries 8 (1): 2–14.
Pilson, M.E.Q. 1991. Aspects of Climate Around Narragansett Bay. NBP-91-64. pp. 59. http://nbep.org/publications/NBP-91-64.pdf. Accessed 19 December 2017.
Pitt, K.A., R.M. Connolly, and P. Maxwell. 2009. Redistribution of sewage-nitrogen in estuarine food webs following sewage treatment upgrades. Marine Pollution Bulletin 58 (4): 573–580.
Poole, H., and W.R.G. Atkin. 1929. Photo-electric measurements of submarine illumination throughout the year. Journal of the Marine Biological Association of the United Kingdom 16 (01): 297–324.
Pruell, R.J., and B.K. Taplin. 2015. Carbon and nitrogen isotope ratios of juvenile winter flounder as indicators of inputs to estuarine systems. Marine Pollution Bulletin 101 (2): 624–631.
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 (6): 612–620.
Pruell, R.J., B.K. Taplin, and K.M. Miller. 2017. Trends in nitrogen isotope ratios of juvenile winter flounder reflect changing nitrogen inputs to Rhode Island, USA estuarine systems. Marine Pollution Bulletin 118 (1-2): 41–47.
Raimonet, M., G. Guillou, F. Mornet, and P. Richard. 2013. Macroalgae δ15N values in well-mixed estuaries: Indicator of anthropogenic nitrogen input or macroalgae metabolism? Estuarine, coastal, and shelf. Science 119: 126–138.
Rudnick, D.T., R. Elmgren, and J.B. Frithsen. 1985. Meiofaunal prominence and benthic seasonality in a coastal marine ecosystem. Oecologia 67 (2): 157–168.
Savage, C., and R. Elmgren. 2004. Macroalgal (Fucus vesiculosus) δ15N values trace decrease in sewage influence. Ecological Applications 14 (2): 517–526.
Schmidt, C.E. 2014. Investigation of nitrogen cycling using stable nitrogen and oxygen isotopes in Narragansett Bay, RI. Dissertation, University of Rhode. Island, Kingston, RI.
Schmidt, C.E., R.S. Robinson, L. Fields, and S.W. Nixon. 2016. Changes to nitrate isotopic composition of waste water treatment effluent and rivers after upgrades to tertiary treatment in the Narragansett Bay watershed, RI. Marine Pollution Bulletin 104 (1-2): 61–69.
Smith, S.V., W.J. Kimmerer, E. Laws, R.E. Brock, and T.W. Walsh. 1981. Kaneohe Bay sewage diversion experiment: Perspectives on ecosystem responses to nutritional perturbation. Pacific Science 35: 279–395.
Spaulding, S.L. and C. Swanson. 2008. Circulation and transport dynamics in Narragansett Bay. In Science for ecosystem-based management Narragansett Bay in the 21st century, ed. A. Desbonnet and B.A. Costa-Pierce, 233–279. New York: Springer.
Thornber, C.S., P. DiMilla, S.W. Nixon, and R.A. McKinney. 2008. Natural and anthropogenic nitrogen uptake by bloom-forming macroalgae. Marine Pollution Bulletin 56 (2): 261–269.
Wells, M.L., G.J. Smith, and K.W. Bruland. 2000. The distribution of colloidal and particulate bioactive metals in Narragansett Bay RI. Marine Chemistry 71 (1-2): 143–163.
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 (1): 144–155.
The late coastal ecologist Scott Nixon was fond of saying that the wise studied lakes, the less-wise studied rivers, where water flowed in one direction, and only the most foolish studied estuaries where water moved in all directions, changing over the course of a day. This has never been truer when trying to assess the impacts of oligotrophication. We would like to thank the Rhode Island Department of Environmental Management for providing hard clams to us for more than a decade. We would also like to thank Mike Charpentier for creating Fig. 1, Steve Granger for the assistance in the field during those first collections in the mid-2000s, and to Scott Nixon and Candace Oviatt for all of the valuable data that they have collected, and information and wisdom that they have provided, over the years. Thanks to Lindsey Fields for measuring the DIN concentrations and Rebecca Robinson for the support to C. Schmidt. We are grateful to Carol Thornber and Lindsay Green of the University of Rhode Island for their help with identifying macroalgae. This manuscript has been improved by input from Roxanne Johnson, Rose Martin, and Brenda Rashleigh. This is ORD tracking number ORD-023673. The views expressed in this article are those of the authors and do not necessarily represent the views or polices of the US Environmental Protection Agency, NEIWPCC, nor of the McLaughlin Research Corporation. Any mention of trade names, products, or services does not imply an endorsement by the US government or the US Environmental Protection Agency. The EPA does not endorse any commercial products, services, or enterprises.
Communicated by Carolyn A. Currin
About this article
Cite this article
Oczkowski, A., Schmidt, C., Santos, E. et al. How the Distribution of Anthropogenic Nitrogen Has Changed in Narragansett Bay (RI, USA) Following Major Reductions in Nutrient Loads. Estuaries and Coasts 41, 2260–2276 (2018). https://doi.org/10.1007/s12237-018-0435-2
- Stable isotope
- Sewage treatment plant
- Wastewater treatment facility
- Tertiary treatment
- Ecosystem response