Published in J. Environ. Qual. 33:124-132 (2004).
© ASA, CSSA, SSSA
677 S. Segoe Rd., Madison, WI 53711 USA
TECHNICAL REPORTS
Ground Water Quality
Assessment of a 
15N Isotopic Method to Indicate Anthropogenic Eutrophication in Aquatic Ecosystems
Marci L. Cole*,a,
Ivan Valielab,
Kevin D. Kroegerc,
Gabrielle L. Tomaskyb,
Just Cebriand,
Cathleen Wigande,
Richard A. McKinneye,
Sara P. Gradyb and
Maria Helena Carvalho da Silvaf
a Save the Bay, 434 Smith St., Providence, RI 02908
b Boston Univ. Marine Program, Marine Biological Laboratory, Woods Hole, MA 02543
c Woods Hole Oceanographic Inst., Woods Hole, MA 02543
d Dauphin Island Sea Lab, P.O. Box 369-370, Dauphin Island, AL 36528
e USEPA, National Health and Environmental Effects Laboratory, Atlantic Ecology Division, 27 Tarzwell Drive, Narragansett, RI 02882
f Univ. de São Paulo, Inst. Oceanográfico, Cidade Univ., Butantã SP, Brazil
* Corresponding author (mcole{at}savebay.org).
Received for publication February 8, 2003.
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ABSTRACT
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Increased anthropogenic delivery of nutrients to water bodies, both freshwater and estuarine, has caused detrimental changes in habitat, food web structure, and nutrient cycling. Nitrogen-stable isotopes may be suitable indicators of such increased nutrient delivery. In this study, we looked at the differences in response of macrophyte 
15N values to anthropogenic N across different taxonomic groups and geographic regions to test a stable isotopic method for detecting anthropogenic impacts. Macrophyte 15N values increased with wastewater input and water-column dissolved inorganic nitrogen (DIN) concentration. When macrophytes were divided into macroalgae and plants, they responded similarly to increases in wastewater N, although macroalgae was a more reliable indicator of both wastewater inputs and water-column DIN concentrations. Smooth cordgrass (Spartina alterniflora Loisel.) 15N increased uniformly with wastewater inputs across a geographic range. We used the relationship derived between S. alterniflora and relative wastewater load to predict wastewater loads in locations lacking quantitative land use data. The predictions matched well with known qualitative information, proving the use of a stable isotopic method for predicting wastewater input.
Abbreviations: ANCOVA, analysis of covariance • DIN, dissolved inorganic nitrogen • NLM, nitrogen-loading model • POM, particulate organic matter
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INTRODUCTION
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INCREASES IN HUMAN POPULATION in coastal watersheds have increased delivery of nutrients to lakes, ponds, and estuaries (Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection, 1990; National Research Council, 1994). The resulting eutrophication has many adverse effects within the estuaries (Duarte, 1995; D'Avanzo et al., 1996; Hauxwell et al., 1998). Increased N loading can lead to blooms of phytoplankton and macroalgae (Duarte, 1995; Hauxwell et al., 1998). These blooms in turn lead to the loss of important estuarine habitats like seagrass meadows. The loss of seagrass meadows is accompanied by the loss of important commercial shellfish and finfish species such as cod (Tveite, 1984), bay scallops (Pohle et al., 1991), and blue crabs (Heck and Orth, 1980). Eutrophic estuaries can also suffer from anoxia (Zimmerman and Canuel, 2000), harmful algal blooms, and brown tides (Hodgkiss and Ho, 1997).
These adverse effects have prompted search for suitable indicators of eutrophication to assess water quality of aquatic ecosystems. Nitrogen-stable isotopes have been suggested as such indicators (Cabana and Rasmussen, 1996; McClelland et al., 1997; McClelland and Valiela, 1998; Lake et al., 2001; McKinney et al., 2001; Wigand et al., 2001; Cole, unpublished data, 2002) for freshwater and estuarine systems.
Differences in ratios of 15N to 14N have been used to define food webs, as well as natural tracers of N sources (Fry and Sherr, 1984; Peterson and Fry, 1987). The ratio of 15N to 14N is expressed as 15N (
) = [(Rsample – Rreference)/Rreference] x 1000, where R is 15N/14N and the reference is atmospheric N2 (Peterson and Fry, 1987). Wastewater N in ground water typically has a 15N of +10 to +22, largely because of denitrification and volatilization of ammonia in septic system leaching fields (Kreitler et al., 1978; Kreitler and Browning, 1983; Aravena et al., 1993; Macko and Ostrom, 1994). This range is significantly higher than the 15N of ground water N derived from atmospheric deposition (+2 to +8; Kreitler et al., 1978; Kreitler and Browning, 1983), and from fertilizer (–3 to +3, Kreitler et al., 1978; Kreitler and Browning, 1983).
The 15N values in primary producers, macrophytes and phytoplankton, reliably reflect N inputs from land to water bodies (McClelland et al., 1997; Voss and Struck, 1997; McClelland and Valiela, 1998; Waldron et al., 2001; Cole, unpublished data, 2002), and also are significantly related to DIN concentrations in the receiving waters (Cole, unpublished data, 2002). Although, 15N of primary producers is more clearly correlated to the percentage wastewater contribution than to N loads (Cole, unpublished data, 2002).
The 15N of primary producers may vary because of differences in taxonomy and geography. Differences in the geographic location of water bodies introduce differences in species composition, climate, and water and sediment characteristics; many of these features could affect the 15N of producers (Peterson and Fry, 1987). Plants acquire N from the sediment, but algae N uptake occurs through fronds (Duarte, 1995). This taxonomic-based contrast may create a different 15N in each producer type since N in sediment and the water column often differ in 15N. The 15N of producers in freshwater and estuaries may also differ because of the marked differences between freshwater and estuarine environments in N supply and in N transformations (Valiela, 1995).
In this report, as a first objective we first test the 15N approach by applying it to a geographically broad range of water bodies to assess how well the N-stable isotopic content of plants, macroalgae, and particulate organic matter (POM) are correlated to two indicators of anthropogenic eutrophication, water-column DIN concentrations, and percentage of land-derived N load that is contributed by wastewater. We use both new and previously collected data to compare producer 15N to percentage wastewater inputs, and to water-column DIN concentrations in fresh and salt water bodies in the U.S. East and West Coasts, and in Brazil. As a second objective, we further extend the use of 15N in macrophytes to predict wastewater inputs to aquatic systems where we lack quantitative information on N or wastewater inputs from land.
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METHODS
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We assessed how the relationship between macrophyte 15N and relative wastewater load changed with different species and with different geographical areas. We first determined how macroalgae and plants responded to wastewater inputs and to water-column DIN concentrations. We then compared species from different geographical areas.
Site Selection
For the expanded geographical test of the 15N method to detect wastewater inputs to receiving waters, we used new data and published data for 31 ponds and estuaries in North and South America (Fig. 1)
. We collected new data from three estuaries (Mashpee River, Great Pond, and Green Pond, MA) and four freshwater ponds (Ashumet Pond, Coonamessett Pond, and Oyster Pond at southwestern Cape Cod and Miacomet Pond at Nantucket, MA). In addition, we collected data from Lamprey River and Oyster River (subestuaries of Great Bay, NH), Nick's Hole and Yent's Bayou (subestuaries of Apalachicola Bay, FL), and Piratininga and Itaipu (two portions of a coastal lagoon system in Brazil). We used previously collected or published data for Sage Lot Pond, Quashnet River, and Childs River, MA; Narragansett Bay, RI; Tijuana Estuary, San Dieguito Lagoon, and Elkhorn Slough, CA; South Slough, OR; and Padilla Bay, WA.
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Fig. 1. Map of North and South America showing locations used in this study. Subestuaries and freshwater ponds of Cape Cod, Great Bay, Narragansett Bay, and Apalachicola Bay are given in Table 1. The number in parentheses indicates number of estuaries or ponds used for each area. If no number is provided, only one estuary was used for that location.
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Table 1. Sites selected, macrophyte 15N, particulate organic matter (POM) 15N, water-column dissolved inorganic nitrogen (DIN) concentrations, and relative contribution of wastewater to modeled land-derived N load for freshwater ponds and estuaries in this study.
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Macrophyte and Particulate Organic Matter 15N Measurements
For the sites in Cape Cod, Great Bay, and Apalachicola Bay in the USA, and Itaipu and Piratininga in Brazil, we collected emergent macrophytes, submergent macrophytes, and macroalgae from up to 10 locations within the freshwater ponds and estuaries (Table 1). Samples from all locations within a water body were combined into one composite sample per pond or estuary. Macrophyte tissues were dried at 60°C for 3 d, ground to a fine powder with a mortar and pestle, and stored in scintillation vials in a dessicator until analysis. The POM was collected in 2-L bottles from three locations around each site, filtered onto ashed glass fiber filters, dried at 60°C for 3 d, and stored in a scintillation vial in a dessicator until analysis. Nitrogen in macrophyte tissue and POM was then analyzed with a Finnigan Delta-S isotope-ratio mass spectrometer (Finnigan Corporation, San Jose, CA) coupled to a Heraeus element analyzer (Heraeus Instruments, Inc., South Plainfield, NJ).
Methods for collection and analysis of samples from Narragansett, RI, and the West Coast estuaries are found in Wigand et al. (2001), Kwak and Zedler (1997), and Fry et al. (2003). The Pacific Coast estuaries received significant freshwater inflow from their watersheds only during certain times of the year (Fry et al., 2003). Since we were most interested in the relationship of macrophyte and POM 15N to actual inputs of land-derived N rather than to N recirculated within the systems, we used only the samples collected at the time of lowest water-column salinity, which corresponded to recent freshwater inflow.
Calculation of Relative Wastewater Load
To determine the contribution of wastewater, fertilizer use, and atmospheric deposition to the total N load to the Cape Cod, Nantucket, and Narragansett Bay sites, we used a nitrogen-loading model (NLM; Valiela et al., 1997, 2000). To apply NLM, we first identified watershed boundaries using water table contours from U.S. Geological Survey maps (Savoie, 1995). We then compiled land uses for each watershed and subwatershed from aerial photos and geographic information system (GIS) software. The land uses were then entered into the NLM to calculate N loads from wastewater, fertilizer use, and atmospheric deposition (Table 1).
Water-Column Dissolved Inorganic Nitrogen Measurements
To compare 15N of macrophytes to ambient concentrations of dissolved inorganic N, we collected water from freshwater ponds and estuaries in Cape Cod, Great Bay, and Apalachicola Bay, and measured NO3 and NH4. We measured NH4 concentrations colorimetrically by the phenol/hypochlorite method (Strickland and Parsons, 1972) or fluorometrically (Holmes et al., 1999). Nitrate concentrations were measured colorimetrically after cadmium reduction to NO2 with either a manual method (Jones, 1984) or with an autoanalyzer (Lachat Instruments, Milwaukee, WI). The values arrived at by this method are actually NO3 + NO2, but because NO2 concentrations are typically an order of magnitude lower than NO3, we refer to this value as the NO3 concentration. For the Brazil lagoons, and the Pacific Coast estuaries, we obtained DIN concentrations from Souza and Wasserman (1997) and Fry et al. (2001).
Statistics
To test whether the 15N values of the macroalgae and plants related differently to wastewater N, we first used an analysis of variance (ANOVA; Statview 5.0.1, SAS, Cary, NC), to test whether the slopes of the two regression lines were significantly different (high F value, low p value). If they were not significantly different, we used an analysis of covariance (ANCOVA; Statview 5.0.1) with N load, wastewater, and DIN concentration as covariates to test if the y-intercepts of each regression line were significantly different (high F value, low p value).
Macrophyte 15N Signatures as Indicators of Percentage Wastewater Inputs
We first regressed macrophyte 15N and wastewater using macrophyte 15N data from both Cape Cod and Narragansett Bay, RI. We then used that relationship to estimate the relative contribution of N by wastewater in estuaries where N loads were not available. For this part of the study, we used measurements of macrophyte 15N from Great Bay, Nick's Hole, Itaipu Lagoon, and Piratininga Lagoon, as well as published data for Tijuana Estuary, San Dieguito Lagoon, Padilla Bay, South Slough, and Elkhorn Slough, and POM 15N data for Yent's Bayou. To check on the plausibility of the prediction, we compiled whatever information was available on the land use and intensity of urbanization of their watersheds, to compare with the magnitude of calculated load.
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RESULTS AND DISCUSSION
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Macrophyte 15N and Relative Wastewater Load and Water-Column Dissolved Inorganic Nitrogen
Regressions were developed to assess how all macrophytes responded to relative wastewater load and to water-column DIN concentrations. We then separated the macrophytes into macroalgae vs. plants and again assessed their relationship to relative wastewater load and to water-column DIN concentrations. Finally, we separated the macrophytes based on geographic location and again developed regressions to assess their relationship to relative wastewater load and to water-column DIN concentrations.
A variety of macroalgae and plants were found in all water bodies sampled (Table 1). The range of 15N values was 0.5 to 13.8, a sufficiently large range for our test to be broadly applicable. The 15N values of macrophytes increased as wastewater, as percentage of the total N load, increased (Fig. 2a
and Table 2). This significant relationship is explained by the fact that wastewater 15N values in ground-water-fed systems are heavier than fertilizer or atmospheric/soil N sources (Pabich et al., 2004). This analysis included many different species in freshwater ponds and estuaries across several geographic regions. Below, we break down this relationship into macroalgae vs. vascular plants, and into different geographic regions. We do not separate freshwater and estuarine species or rooted vs. nonrooted species since Cole (unpublished data, 2002) showed no difference in response of 15N values between these different groups of macrophyte species at Cape Cod.
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Table 2. Regression statistics for linear regression between macrophyte 15N and wastewater as a percentage of N load for Cape Cod and Rhode Island separately and combined. Data for Cape Cod is from Cole (unpublished data, 2002). Data for Rhode Island is from Wigand et al. (2001) and McKinney (unpublished data, 2001).
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Macrophyte 15N increased significantly as DIN in water from the estuaries where the collected producers increased (Fig. 2b and Table 3). In this case, the scatter of points was larger than for wastewater N. Nonetheless, on aggregate, N isotopic signatures did reflect ambient DIN concentrations in the estuaries. Lake et al. (2001) found a similar logarithmic relationship between consumers and water-column DIN concentrations in freshwater ponds. The 15N of producers can be affected by the concentration of DIN in the water column, regardless of its source. Higher water-column concentrations lead to high rates of N isotopic fractionation when producers assimilate DIN (Wada and Hattori, 1978; Fogel and Cifuentes, 1993), but this fractionation leads to lighter producer isotopic values. Thus, the increase of producer 15N values with DIN concentrations is less marked at higher concentrations (Cabana and Rasmussen, 1996; Lake et al., 2001). Macrophyte 15N values, then, are sensitive mainly to low DIN concentrations. Although there is a significant relationship between macrophyte 15N values and water-column DIN concentrations, the overall poor R2 of 0.14 suggests that the relationship may not be a particularly useful predictor.
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Table 3. Regression statistics for linear regression between macrophyte 15N and water-column DIN concentrations. Data and sources listed in Table 1.
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Both macroalgae and plant 15N values significantly increased as wastewater N increased as a portion of the total N load (Fig. 3a and Table 2). There was no statistical difference by ANCOVA between the slopes and intercepts of the two regressions. Plants had a larger range of 15N values (0.5–13.8) than macroalgae (4.9–9.9), but this difference was likely due to the sampling of many more plant species than macroalgae. One might expect differing responses of macroalgae and plants to increases in wastewater N because of differences in N uptake rates in preference for NO3 or NH4 in internal N cycling rates and in N sources. Plants have access to porewater N and water-column N, while macroalgae can take up N only from the water column. Despite these complex factors, there was no difference in slope (F = 0.2, not significant) or y-intercept (F = 0.39, not significant) in the two responses of macroalgae and plants to increases in wastewater load. In summary, although both relationships are good, the macroalgae relationship is tighter. This suggests that when macrophytes are separated into vascular and nonvascular groups, nonvascular macroalgal 15N values would be a better predictor of wastewater N.
Macroalgal 15N values increased significantly with water-column DIN concentrations, while plant 15N values did not (Fig. 3b and Table 3). The two regressions had similar slopes. Macroalgae may respond significantly because they only have access to water-column DIN, but plants have access to ground water and porewater N and therefore may not be coupled to the water-column N. In summary, macroalgae are better indicators of the water-column DIN concentrations than plants.
In different estuaries with a range of watershed land uses, S. alterniflora 15N values responded similarly to wastewater inputs (Fig. 4
, statistics in Table 2). As wastewater input increased, S. alterniflora 15N values for both geographic areas were significantly enriched in 15N. Lake et al. (2001) found a similar response of freshwater pond sediment and consumer 15N relative to the fraction of residential land in pond watersheds. Although the relationships for the two geographic regions (Cape Cod and Rhode Island) had the same slope, the regressions were offset by a small amount, 1.3. This minor difference is likely due to differences in estuary processing between the two regions. Regardless, the regressions of one plant species, S. alterniflora, to wastewater inputs calculated for two different geographic regions were not different (F = 0.14, not significant).
To further analyze the geographical differences we grouped macrophyte 15N values into different geographic regions, and correlated the 15N signatures vs. the water-column DIN concentrations (Fig. 4b). The Pacific estuaries had high DIN concentrations, but macrophyte 15N values spanned nearly the same range as those in the northern Atlantic and Brazilian estuaries. These Pacific estuaries have limited inflow of freshwater, so we used data only from seasons with freshwater inflow to best capture inputs from land. Fry et al. (2003) attribute high concentrations during the high flow season to direct agricultural runoff and sewage effluent. The Brazilian lagoon water-column DIN concentration values fell between those of the Pacific and north Atlantic regions. The two Gulf of Mexico estuaries had low 15N values and low DIN concentrations. Both estuaries are fairly pristine with relatively undeveloped watersheds.
Particulate Organic Matter 15N and Relative Wastewater Load and Dissolved Inorganic Nitrogen Concentrations
The POM 15N values were significantly related, although with large scatter, to percentage wastewater in Cape Cod water bodies, but the relationship was not significant when Narragansett Bay data were included (Fig. 5a)
. The POM 15N values were not significantly related to water-column DIN concentrations (Fig. 5b). This is contrary to findings of Cole (unpublished data, 2002), where data from a more geographically restricted area showed that 15N values were related logarithmically to water-column DIN concentrations in Cape Cod water bodies.
The 15N values of POM seem to be less reliable indicators of land-derived N than those of macrophytes. In fact, changes in phytoplankton community structure across time may occur, and different species may fractionate N to different degrees. For example, cyanobacteria blooms induce lower 15N values in water-column DIN (Peterson and Fry, 1987; Fogel and Cifuentes, 1993; Kendall, 1998). The POM includes not only phytoplankton, but also particles from sediments, aggregates of DOM, macrophytes, or terrestrial origin. New methods have recently been developed to assess 15N values of phytoplankton chlorophyll (Sachs et al., 1999; Sachs and Repeta, 2000). The new methods were developed too recently to be of use to this study, but future studies could incorporate them to better assess the relationship between phytoplankton 15N values and land-derived N.
Use of 15N of Macrophytes to Estimate Percentage Wastewater Inputs
The relationship of 15N of macrophytes to percentage wastewater, defined in Fig. 2, was sufficiently good that we ventured to use that relationship to estimate the percentage wastewater N for estuaries for the estuaries where data were unavailable (Lamprey River and Oyster River, NH; Nick's Hole and Yent's Bayou, FL; Piratininga Lagoon and Itaipu Lagoon, Brazil; Tijuana Estuary, San Dieguito Lagoon, and Elkhorn Slough, CA; Padilla Bay, WA; and South Slough, OR). We could not directly verify these 15N-based estimates to measurements, but we could compare the estimates of wastewater N to available qualitative information on watershed land use for each of these estuaries.
In general, the estimated wastewater percentages matched what is known of watershed land uses for those estuaries (Table 4). In all cases, estimated wastewater percentages were high (62–114%) where there were wastewater inputs from septic systems, wastewater treatment plant outfalls, cattle grazing, or direct releases of raw sewage. Where the watershed had little development, the estimated wastewater percentages were low (0–32%). These comparisons suggest that the 15N method might be useful where N-load estimates might not be available.
Estimates of the percentage of wastewater N based on macrophyte 15N may be inaccurate if other N sources have a strong effect on 15N values of macrophytes. The wastewater estimates may be too high if N sources with heavy 15N signatures such as coastal upwelling and regeneration contribute a significant proportion of the N available to macrophytes. Fry et al. (2003) suggest that agricultural runoff in regions with high rates of soil denitrification may have 15N values close to that of wastewater. The wastewater percentage might be underestimated if sources of N with light 15N signatures, such as atmospheric deposition, N2 fixation, and nitrification (Kendall, 1998), are available in the water column for producer uptake. In spite of these caveats, the method using macrophyte 15N to identify relative inputs of land-derived wastewater worked well in the sites of this study.
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CONCLUSIONS
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Macrophyte 15N was a reliable indicator of relative wastewater load to receiving waters and, to a lesser extent, of water-column DIN across a wide geographic range. The stable isotope method for detecting wastewater works equally well for macroalgae and plants across different geographic regions, while macroalgal 15N values were a better tracer of water-column DIN concentrations than vascular plants. This stable isotopic method can detect wastewater and DIN at low and high levels, making it useful for identifying incipient eutrophication before water bodies begin to show effects of eutrophication. The results for this research provide an inexpensive and simple tool to assess effects of watershed urbanization on coastal water bodies. For example, the derived relationship between Spartina 15N and percentage of wastewater is currently being used in the assessment of the N source for a large noxious macroalgal bloom in a small Rhode Island estuary with a relatively undeveloped watershed. The results of this assessment will help determine a restoration plan for the estuary. This is just one example of the possible uses of this stable isotope method.
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ACKNOWLEDGMENTS
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This work was supported by funds from the Woods Hole Oceanographic Institution Sea Grant Program to Ivan Valiela, from the Cooperative Institute for Coastal and Estuarine Environmental Technology to Ivan Valiela, and from Massachusetts Department of Environmental Protection to Applied Science Associates, Narragansett, RI, and Ivan Valiela. This work is the result of research sponsored by NOAA National Sea Grant College Program Office, Department of Commerce, under Grant no. NA86RG0075; and Woods Hole Oceanographic Institution Sea Grant Project no. R/M-40. The U.S. Government is authorized to produce and distribute reprints for governmental purposes notwithstanding any copyright notation that may appear hereon.
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INTRODUCTION
