Nitrogen-stable isotope signatures in estuarine food webs: A record of increasing urbanization in coastal watersheds

Nutrient enrichment as a result of anthropogenic activity concentrated along the land-sea margin is increasing eutrophication of near-shore waters across the globe. Management of eutrophication in the coastal zone has been ’ hampered by the lack of a direct method to trace nitrogen sources from land into coastal food webs. Stable isotope data from a series of estuaries receiving nitrogen loads from 2 to 467 kg N ha’ yr-’ from the Waquoit Bay watershed, Cape Cod, Massachusetts, indicate that producer and consumer 15N-to-14N ratios record increases in wastewater nitrogen inputs. Nitrate from groundwater-borne wastewater introduces a ‘“N-enriched tracer to estuaries. This study explicitly links anthropogenically derived nitrogen from watersheds to nitrogen in estuarine plants and animals, and suggests that wastewater nitrogen may be detectable in estuarine biota at relatively low loading rates, before eutrophication leads to major changes in species composition and abundance within estuarine food webs. Eutrophication caused by increased anthropogenic nitrogen inputs is a major mechanism altering coastal habitats worldwide (Sand-Jensen and Box-urn 1991; Duarte 1995; GESAMP 1990; NAS 1994). A variety of indexes have been developed to quantify the extent of eutrophication brought about by N loading (Schmitt and Osenberg 1995). Most of these indexes make use of taxonomic shifts and changes in abundance of producers and consumers resulting from eutrophication. Such indicators, although useful, provide an a posteriori assessment of eutrophication; they depend on changes that have already taken place in the biota. Restoration of habitats already altered by eutrophication is difficult, so methods that detect increases in nutrient loads while they are still relatively low would be welcome tools for coastal habitat management. In addition, identification of N sources would make management responses more effective. The use of N stable isotope ratios to track anthropogenic N directly into estuarine food webs may, for the first time, provide a method to detect incipient eutrophication, as well as identify the responsible source. The stable isotopes 14N and 15N occur overall on earth in a fixed proportion of approximately 273 14N atoms for each 15N atom, while the ratio of 15N to 14N differs among specific N pools in the environment (Peterson and Fry 1987). Although the absolute magnitude of natural variation in N-stable isotope ratios in the environment is small, N isoAcknowledgments Grants from the NSF Land Margin Ecosystems Research, EPA Region 1, NOAA Sanctuaries and Reserves, NOAA Coastal Oceans, and WHO1 Sea Grant programs supported this work. We thank staff of the Waquoit Bay National Estuarine Research Reserve and L. Saucy for technical support, B. Peterson and A. Giblin for their comments on earlier versions of this manuscript, and B. Lapointe and B. Fry for critical review of this manuscript. We are grateful to Trish and David Palmer for providing graduate student support through the Waquoit Bay Fellowship. topic signatures from different pools are often quit distinct, making N sources identifiable and traceable within an ecosystem. N-stable isotope data are typically normalized relative to the 15N/14N of atmospheric N, as 6*“N (%;o) = [(Rsamplcl Rtrn) 1 ] X IO” (Peterson and Fry 1987). In areas with sandy unconsolidated aquifers such as Cape Cod, Massachusetts, watershed sources of N are delivered to estuaries almost exclusively via groundwater flow (Valiela et al. 1992). Groundwater studies have used natural abundance stable isotope signatures of NO,to help identify the major sources of N (wastewater, fertilizer, and atmospheric deposition) to aquifers (Kreitler et al. 1978; Gormly and Spalding 1979; Kreitler 1979; Aravena et al. 1993). Groundwater influenced only by atmospheric deposition typically bears NO,--S15N values ranging from +2 to +8%0, while NO,derived from human and animal wastes is more enriched in 15N (+ 10 to +20%0), and nitrate from synthetic fertilizers is more depleted in 15N (-3 to +3%0). Elevated S15N values in groundwater generated from human and animal wastes are attributed to volatilization of 14N-rich ammonia during early stages of wastewater degradation, as well as microbial processes acting on wastewater N before it reaches the aquifer (Macko and Ostrom 1994). The low S15N values associated with synthetic fertilizers are due to the conversion of atmospheric N, during manufacturing (Freyer and Aly 1974; Gormly and Spalding 1979). Physical and biological processes that fractionate N can make it difficult to precisely quantify N contributions from different sources (Hauck et al. 1972; Bremner and Tabatabai 1973; Hauck 1973; Mariotti et al. 1988), particularly for studies that rely only on absolute stable isotope values to assess source contributions. Comparisons of S15N values in groundwater from aquifers with potential anthropogenic N loads to groundwater S15N from relatively pristine locations have, however, produced valuable information on source contributions (Kreitler et al. 1978; Gormly and Spalding 1979; Kreitler 1979). With this comparative approach, dif-