Foraging habitat use by colonial waterbirds breeding in New York Harbor was examined to identify resources that were particularly important for the provisioning of young. Stable isotope values of carbon, nitrogen, and sulfur were measured in nestling waterbird feathers to determine the habitat type (ranging from marine to freshwater and anthropogenic) in which adults primarily foraged. Six species were investigated: Black-crowned Night-Herons (Nycticorax nycticorax), Great Egrets (Ardea alba), Glossy Ibises (Plegadis falcinellus), Double-crested Cormorants (Phalacrocorax auritus), Great Black-backed Gulls (Larus marinus), and Herring Gulls (L. argentatus). Waterbird populations exhibited both inter- and intra-specific variation in stable isotope values (P < 0.001), indicating variation in foraging habitat use among focal species across the estuary. Therefore, depending on the species-and region-specific conservation goal, management strategies would potentially need to target very different foraging habitats for protection and remediation. For instance, habitat use by Double-crested Cormorants closely reflected available habitat near nesting colonies, while Glossy Ibises used primarily freshwater resources at one colony and marine resources at another, despite the fact that both colonies were located in marine environments. Great Egrets and Double-crested Cormorants both showed significant regional variation in isotopic niche size, and both species of gulls (considered to be generalist scavengers) were found to have isotopic niche sizes reflecting a specialist diet. Stable isotope analysis of nestling feathers provided novel information about the foraging resources that were most important to waterbirds in regions across the harbor.
The New York/New Jersey Harbor Estuary (hereafter the harbor) has an area of approximately 40,000 km2 and provides a mosaic of urban habitat types for wildlife, including open water, freshwater and saltwater marsh, uplands, and the built environment. Small, abandoned islands in the harbor have become important breeding areas for many of New York State's waterbirds since their resurgence in the region in the 1970s (Harbor Herons Subcommittee 2010). Sixteen waterbird species have been known to reproduce on these islands and forage in the surrounding wetlands and waterways to feed themselves and provision their young (Craig 2012). Current knowledge and conservation efforts for these birds have generally focused on breeding population sizes and nesting phenology. However, the Harbor Heron Conservation Plan of the New York/New Jersey Harbor Estuary Program has recently called for research to expand our understanding to include the foraging behavior of waterbirds in this system (Harbor Herons Subcommittee 2010). To this end, we investigated foraging resource use through stable isotope analysis (SIA) of nestling waterbird feathers.
Stable isotope analysis of feathers reflects a bird's diet over the timescale of feather growth, and contains information about the relative importance of foraging resources during that period (Hobson and Clark 1992; Hobson 1999; Inger and Bearhop 2008; Bond and Jones 2009). Feathers from nestling birds in particular integrate the resources with which adult birds have provisioned their young, and are therefore most suitable for answering questions about local foraging behavior and diet on the breeding grounds (Cherel et al. 2000). Stable isotope values measured in a population (expressed in δ notation as parts per thousand; ‰) can be considered to describe an isotopic niche, analogous to the n-dimensional hypervolume of the ecological niche (Hutchinson 1957). The isotopic niche is defined as an area in δ-space (‰2) with isotopic values as coordinates (Newsome et al. 2007).
Isotopic values of carbon (δ13C), nitrogen (δ15N), and sulfur (δ34S) can be used to monitor diet, relative trophic position, and foraging habitat of birds (Bond and Jones 2009). δ13C values indicate the extent of freshwater or marine resource use, with more negative (lower) values indicating more freshwater resource use, and less negative (higher) values indicating more marine resource use (Mizutani et al. 1990; Hobson and Clark 1992; Bearhop et al 1999; Bond and Jones 2009). Higher δ13C values can also result from inclusion of C4 photosynthetic plant materials, such as foods containing corn or cane sugar, in the diet (Farquhar et al. 1989). In waterbirds, this indicates consumption of anthropogenic resources such as human food waste or intensive aquaculture (Hebert et al. 2009). When anthropogenic resource use is suspected, δ34S can be added to the analysis, as this isotope provides a more straightforward measure of marine vs. fresh-water resource use that is not influenced by anthropogenic foods (Lott et al. 2003). δ15N values primarily indicate the relative trophic position at which a bird has foraged (Steele and Daniel 1978; Minagawa and Wada 1984; Hobson and Clark 1992; Bond and Jones 2009).
Six waterbird species were investigated in this study, including three species of long-legged wading birds: the Black-crowned Night-Heron (Nycticorax nycticorax), Great Egret (Ardea alba), and Glossy Ibis (Plegadis falcinellus); one species of diving bird: the Double-crested Cormorant (Phalacrocorax auritus); and two gull species: the Great Black-backed Gull (Larus marinus) and Herring Gull (L. argentatus). These six species were the most numerically abundant waterbirds nesting in the harbor during this study, and were selected to span the range in phytogeny, conservation status, and foraging strategy within the harbor's waterbird community (Craig 2012). In general, long-legged wading birds (ibises, egrets, and night-herons) capture fish, crabs, amphibians, and aquatic invertebrates by wading into shallow waters and marshes (Davis and Kricher 2000; McCrimmon et al. 2001; Hothem et al. 2010); cormorants dive to capture live prey (primarily fish; Hatch and Weseloh 1999); and gulls scavenge for a variety of items ranging from fish to human garbage (Pierotti and Good 1994; Good 1998).
The objectives of this study were to examine foraging habitat use of a suite of waterbird species nesting within the harbor, and to identify the habitats that were particularly important among waterbird populations and across regions. We formulated three specific hypotheses: 1) that cormorants would have the highest correlation between nearby habitat availability and habitat use, as these birds can dive for prey in waters immediately surrounding their nesting habitats regardless of shoreline topography; 2) that long-legged wading birds would display broader resource use and larger isotopic niche size, particularly on islands that lacked shorelines with suitably shallow foraging habitat; and 3) that gulls would exhibit the largest isotopic niche size, as these birds are known to be primarily generalist scavengers.
This study was conducted across five islands in the harbor (Fig. 1): two in Lower Bay (Hoffman and Swinburne Islands), one in the East River (South Brother Island), and two in Jamaica Bay (Canarsie Pol and Elder's Point Marsh). These three focal regions (Lower Bay, the East River, and Jamaica Bay) were chosen because they contain the three largest and most diverse waterbird colonies in the harbor, and because they encompass a variety of aquatic habitat types ranging from brackish and freshwater tributaries to marine. Public access to all islands is restricted for the protection of waterbirds.
Hoffman and Swinburne Islands are manmade islands located off the east shore of Staten Island, New York (40° 34′ 43.38″ N, 74° 3′ 13.51″ W) in Lower Bay. Aquatic habitat in Lower Bay is primarily marine, as the bay opens onto the Atlantic Ocean. Canarsie Pol (40° 37′ 16.03″ N, 73° 52′ 23.88″ W) and Elder's Point Marsh (40° 38′ 9.97″ N, 73° 50′ 55.50″ W) are natural islands situated in the northwest region of Jamaica Bay. As in Lower Bay, aquatic habitat in Jamaica Bay is primarily marine, as the bay opens onto the Atlantic Ocean. South Brother Island (40° 47′ 46.00″ N, 73° 53′ 53.02″ W) is a natural island situated between Riker's Island and the Bronx, New York. Aquatic habitat near South Brother Island ranges from brackish to freshwater.
In June and July of 2009 through 2012, waterbird nestlings of each species were captured by hand at nesting colonies (Table 1). Between one and 10 contour feathers per individual were collected while the nestlings were handled for banding. In addition, between June and September of each year, contour feathers were collected from recently deceased water bird nestlings of known species identity encountered on each island. All feather samples were stored in labeled paper envelopes and classified by species and location.
Stable Isotope Analysis
All feather samples were analyzed for δ13C and δ15N. A 1-mg sample (± 0.1 mg) of each feather was encapsulated in tin and analyzed for δ13C and O15N using a Thermo Finnigan Delta V Advantage isotope ratio mass spectrometer interfaced to a NC2500 elemental analyzer. One internal laboratory standard of American mink (Neovison vison) tissue was analyzed for every 10 unknowns. A chemical methionine standard was used to measure instrumental accuracy across a gradient of amplitude intensities. Isotope corrections were performed using a two-point normalization (linear regression) of all raw δ13C and δ15N data with two additional in-house standards: Cayuga Lake brown trout (Salmo trutta) and corn (Zea mays). Based on standard deviations of withinrun replicate measurements of standards, analytical error was estimated to be ± 0.2%o for δ13C and ± 0.3‰ for δ15N.
A subset of Herring Gull samples (n = 5) was also analyzed for δ34S to explore the potential for anthropogenic contributions to diet. For these individuals, a 1-mg sample (± 0.1 mg) of each feather was encapsulated in tin and analyzed for δ34S using an isotope ratio mass spectrometer interfaced to an elemental analyzer. Internal laboratory standards were analyzed for every 10 unknowns. Based on standard deviations of within-run replicate measurements of standards, analytical error was estimated to be ± 0.3‰ for δ34S. Results are relative to international standards of PeeDee Belemnite for carbon, atmospheric air (N2) for nitrogen, and Vienna Canyon Diablo Troilite for sulfur.
Regional comparisons of mean ± SD δ13C and δ15N of feathers sampled from colonial waterbird nestlings of six species in three regions of the New York Harbor estuary (June to September 2009–2012). Regions followed by different superscript letters signify significant intraspecific differences according to the Tukey-Kramer honest significant difference (HSD) test.
Single-factor multivariate analysis of variance (MANOVA) and post-hoc analysis of variance (ANOVA) with the Tukey-Kramer honest significant difference (HSD) test were used to determine statistically significant variation in δ13C and δ15N values using a factor of nesting location or species depending on the analysis. A MANOVA of δ15C and δ15N was conducted using either mortality or year (by species) as the single factor to confirm that isotope values did not differ significantly between live and dead birds (Vasil et al. 2012) or across sampling years. The δ13C and δ15N values of feathers collected from live vs. dead nestlings and across multiple years were not found to differ significantly (P > 0.05); therefore, the data were analyzed regardless of mortality or collection year for all subsequent analyses. These statistical analyses were performed using JMP statistical software (SAS Institute, Inc. 2012).
When interpreting stable isotope results, we drew very conservative conclusions regarding relative trophic position from δ15N values, as baseline δ15N information was unknown in this system (Post 2002). Further caution was taken when comparing isotope values among multiple species, as the diet-tissue discrimination factors of many of these species are unknown (Bond and Diamond 2011). We only considered inter-specific isotopic differences greater than the standard deviation of discrimination factors of bird feathers (approximately 1.5‰ for carbon and 1.1 ‰ for nitrogen; Caut et al. 2009) to reflect differences in diet and foraging behavior among species.
Isotopic niche size (‰2) of each waterbird population was calculated with the Stable Isotope Analysis in R (SIAR) package (R Development Core Team 2014) using a Bayesian approach to estimate standard ellipse area (SEAB) of the δ15C and δ15N data (Jackson et al. 2011). This approach was chosen as it is well suited for small sample sizes, and it provides a measure of uncertainty around the estimated isotopic niche size allowing for statistical comparisons. The number of posterior draws in the model was set at 106.
The waterbird community exhibited both inter- and intra-specific variation in δ13C and δ15N (whole MANOVA model: F8,277 = 38.25, P < 0.001). For each species discussed below, isotopic values are reported as mean ± SD of δ13C and δ15N (Table 1), and isotopic niche sizes are reported as the mode of the SEAB posterior distribution (Fig. 2).
Of the three long-legged wading birds sampled in this study, only the Black-crowned Night-Heron exhibited no regional isotopic variation. Average δ15N values for the Black-crowned Night-Heron were relatively high (14.7 ± 2.1‰ and 14.3 ± 1.2‰ Table 1) in both sampled regions, Lower Bay and the East River, respectively. Average δ13C values were also regionally similar, and the range in δ13C (from -25.8‰ to -14.8‰) suggested a broad mix of resource use from freshwater/ brackish and marine habitats. This species foraged in a moderate sized isotopic niche in comparison to other long-legged wading birds (9.3‰2 in Lower Bay and 7.7‰2 in the East River), and exhibited no significant regional variation in isotopic niche size (Fig. 2).
Great Egrets and Glossy Ibises both exhibited regional variation in isotope values (P < 0.001 for both species). Similar to Black-crowned Night-Herons, Great Egrets from Lower Bay and the East River had relatively high average δ15N values (14.4 ± 1.7‰ and 14.8 ± 2.1‰, respectively; Table 1), and a similar range of δ13C values (from -25.3‰ to -13.7‰) with little regional variation. However, Great Egrets sampled from Jamaica Bay exhibited higher δ13C values on average (Table 1), and ranged from -19.6‰ to -13.3‰, indicating a greater proportion of marine resource use. Great Egrets also showed significant regional variation in isotopic niche size (Fig. 2), with a relatively large isotopic niche in the East River (15.4‰2), an intermediate-sized isotopic niche in Lower Bay (8.6‰2, smaller than the East River; P = 0.01) and a small isotopic niche in Jamaica Bay (4.3‰2, smaller than Lower Bay; P = 0.01; Fig. 2).
Glossy Ibises were sampled in Lower Bay and Jamaica Bay (they did not nest in the East River during the sampling period), and exhibited isotopic variation between these regions (P < 0.001). This species had relatively low δ15N values in both regions (8.0 ± 2.1‰ in Lower Bay and 10.5 ± 1.6‰ in Jamaica Bay), and, in fact, exhibited the lowest δ15N values of the six species in this study. While ibises sampled from Jamaica Bay had δ13C values within the range observed in other long-legged wading birds (from -20.9‰ to -16.1‰), the values observed in Lower Bay (ranging from -27.4‰ to -19.2‰) were significantly lower on average (-24.7 ± 2.1‰; P < 0.001; Table 1), indicating a greater pro-portion of freshwater resource use. This species exhibited no regional variation in isotopic niche size, with a moderate-sized isotopic niche in Lower Bay (10.4‰2) and in Jamaica Bay (4.4‰2) (Fig. 2).
Double-crested Cormorants exhibited isotopic variation among all three focal regions (P < 0.001; Table 1). Relatively high δ13C values were observed in birds from Jamaica Bay (from -15.1‰ to -14.2‰), indicative of a predominantly marine diet. Cormorants from Lower Bay had a broader δ13C range (from -22.1‰ to -15.2‰) similar to that observed in Black-crowned Night-Herons and Great Egrets from this region. East River cormorants exhibited an even broader range (from -28.3‰ to -15.6‰) and lower average δ13C value (-20.5 ± 3.8‰; Table 1), suggesting a greater contribution of freshwater resources than observed in the other two regions. Average δ15N values were relatively high (from 15.0 ± 1.7‰ to 15.6 ± 1.0‰; Table 1) and similar among regions. As observed in Great Egrets, the Double-crested Cormorants nesting in the East River had a larger isotopic niche (16.7‰2; P < 0.001) than those observed in the other two nesting regions (3.2‰2 in Lower Bay and 0.8‰2 in Jamaica Bay). The isotopic niche size in Lower Bay was in turn larger than that observed in Jamaica Bay (P < 0.001), although by a far narrower margin (Fig. 2).
The Great Black-backed Gull was only sampled in one location (Lower Bay), while the Herring Gull was sampled in Lower Bay and Jamaica Bay. Great Black-backed Gulls exhibited the highest average δ15N value observed in this study (15.9 ± 1.2‰; Table 1). The δ13C values were also relatively high (ranging from -17.6‰ to -15.9‰), indicating a predominantly marine diet. Interestingly, despite its reputation as a generalist scavenger, this species exhibited a very small isotopic niche (1.9‰2). The Herring Gull showed no regional isotopic variation. It had lower average δ15N values than the Great Black-backed Gull (12.7 ± 1.3‰ and 12.8 ± 1.3‰; Table 1), but similar δ13C values (ranging from -19.1‰ to -15.8‰). Sulfur SIA was conducted on a subset of Herring Gull feathers from Jamaica Bay and Lower Bay to investigate potential anthropogenic resource use. SIA yielded an average δ34S value of 10.0 ± 2.1‰, a lower value than would be expected in a marine-foraging bird (Lott et al. 2003). Interestingly, Herring Gulls also had a very small isotopic niche (2.2‰2 in Lower Bay and 2.7‰2 in Jamaica Bay), with no regional variation (Fig. 2).
The stable isotope approach used in this study allowed us to evaluate differences in foraging ecology among species nesting in three regions of the harbor, and identify the habitat types that were most important in the diet of individual populations within this urban estuary. Waterbird populations exhibited both inter- and intra-specific variation in δ13C and δ15N, indicating differences in foraging habitat use among regions and species. While it is not surprising to find differences in isotopic values among species with differing foraging ecologies (Inger and Bearhop 2008), these findings suggest that, depending on the species- and region-specific conservation goal, management strategies would potentially need to target very different foraging habitats for protection and remediation.
Double-crested Cormorants from Lower Bay and Jamaica Bay had δ13C values indicative of a predominantly marine diet, and suggested that birds likely foraged in the bays surrounding their respective nesting colonies as well as the coastal Atlantic Ocean. Cormorants from the East River exhibited a lower average δ13C value, indicating a greater contribution of freshwater resources than observed in the other two regions. This is consistent with the brackish/freshwater environment surrounding the East River colony. Cormorants nesting in the East River also exhibited a larger isotopic niche than those observed in the other two nesting regions (five times the range observed in Lower Bay and 20 times that observed in Jamaica Bay), indicating that a wider range of foraging habitats and prey items contributed to the diet of these birds. This observation may reflect the diverse nature of foraging habitat availability in the East River and its freshwater tributaries. Alternatively, birds nesting at this location might have foraged at greater distances from the colony to meet their metabolic needs and those of their young, as the area surrounding this colony is highly developed and industrial. The resulting increased foraging distance would also explain the large range of δ13C values (the largest range observed in this study).
As anticipated, Black-crowned Night-Herons exhibited a large range in δ13C values and relatively large isotopic niches in both Lower Bay and the East River. As longlegged wading birds, their foraging strategy may have required them to forage at greater distances from their colony sites, exposing them to a large and overlapping range of foraging habitats.
In contrast to Black-crowned Night-Herons, Great Egrets had a significantly larger isotopic niche in the East River than in Lower Bay. The isotopic niche size was likely influenced by the same factors proposed for cormorants. Egrets in Jamaica Bay exhibited very high δ13C values suggesting a primarily marine diet. Together with a small isotopic niche, the data suggest that egrets nesting in Jamaica Bay likely also foraged in Jamaica Bay. This conclusion is supported by the presence of extensive suitable saltwater marsh and sandy beach habitat in this region.
Glossy Ibises exhibited a similar pattern in Jamaica Bay, with δ13C values suggesting a primarily marine diet, and a relatively small isotopic niche, together indicating that these birds likely remained in Jamaica Bay to forage. Ibises in Lower Bay exhibited significantly lower δ13C values suggesting that, despite the absence of freshwater resources surrounding their nesting colony, freshwater foraging habitats were the most important habitat type for this population during chick rearing. Their use of freshwater resources to feed their growing nestlings is consistent with studies conducted on White Ibis (Eudocimus albus) in Florida (Bildstein 1993). As with the other long-legged wading birds, it is not surprising that Glossy Ibises from Lower Bay would travel some distance from their nesting colony to forage, as the nesting islands in this region are manmade with steep stone shorelines unsuited for their foraging strategy. The observation that ibises from Lower Bay and Jamaica Bay used vastly different foraging habitat types and prey base is novel, and has not been suggested by observational methods. Ibises from both regions exhibited the lowest δ15N values of the six focal species in this study. These low δ15N values might have derived from a difference in source nitrogen in foraging habitats used by ibises, but most likely indicated that these birds generally relied on prey of a low relative trophic position. This is supported by the general foraging strategy of ibises, which, unlike egrets and night-herons, tend to forage by probing for invertebrates in shallow water, fields, and marshes (Davis and Kricher 2000).
Contrary to our expectation, gulls had among the smallest isotopic niches in this study. Interestingly, the Great Black-backed Gulls observed in Lower Bay exhibited δ13C and δ15N values very similar to those observed in cormorants in the same region (Table 1). The general understanding of the foraging strategies of cormorants (diving predators) and gulls (generalist scavengers) does not explain this similarity. Great Black-backed Gulls, however, have been known to exhibit predatory behavior (Good 1998), and were observed during this study consuming cormorant eggs and young when the cormorant colonies were disturbed. While it is possible that these species were eating different food sources with the same isotope value, we believe that the similarity was due to gulls consuming a combination of cormorant eggs and young, and scavenging for food scraps in the understory beneath the cormorant colony. Regardless of the specific scavenging or predatory behavior, our results suggest that cormorant-related diet items may be the most important food source for Great Black-backed Gulls nesting in Lower Bay. This specialized diet would explain the small isotopic niche observed in this species.
Herring Gulls sampled in both Lower Bay and Jamaica Bay exhibited relatively high δ13C values (similar to those observed in the Great Black-backed Gull) but relatively low δ15N values (Table 1). These δ15N values might be explained by the scavenging of fish from lower trophic positions in a marine environment, although there is no simple mechanism for a generalist scavenger to specialize in lower trophic position carrion. This hypothesis was further undermined by sulfur SIA of a subset of Herring Gull feathers that yielded an average δ34S value lower than would be expected in a marine-foraging bird (Lott et al. 2003). The most likely explanation for the isotopic values observed in Herring Gulls is anthropogenic resource use. Scavenging of human food waste could lead to the observed high δ13C values through the consumption of C4 photosynthetic plant materials such as cron-and cane sugar-based foods, as well as the relatively low δ34S values due to the use of fresh water in agriculture. Such resource use could also lead to the lower observed δ15N values due to the relatively low trophic position of these diet items. The distribution of isotope values in Herring Gulls from Lower Bay and Jamaica Bay overlapped to an extent not observed in any other focal species suggesting that Herring Gulls exhibited little to no regional variation in foraging habitat use. With the additional evidence of small isotopic niche, suggesting limited variation in the diet, we conclude that anthropogenic foods were likely the primary resource used by Herring Gulls provisioning their young in both nesting regions sampled in this study.
Overall, SIA of nestling feathers provided novel information about the foraging resources that were most important to waterbirds in regions across the harbor, and should be used in the identification and prioritization of foraging habitats based on their importance to species of conservation concern. However, SIA alone cannot clearly distinguish among multiple foraging sites where similar foraging habitat types are available. Monitoring and tracking methods such as radio- and satellite-telemetry can provide information about physical locations frequented by individuals of a population, and can be used to compile the suite of sites for potential protection or remediation. Stable isotopes can then be used to prioritize foraging habitats based on the relative importance of the resources they provide, and also to modify and focus monitoring efforts on habitat types known to be of particular importance to a focal population. An integrative approach of observational methods and SIA will therefore facilitate both the identification of a suite of potential foraging sites, and the prioritization of those sites for waterbird conservation.
We would like to thank the National Park Service and the New York City Department of Parks and Recreation for access to protected colonial waterbird nesting islands throughout New York Harbor. Samples were analyzed at Cornell University's Stable Isotope Laboratory (δ13C and δ15N) and the University of Utah's Stable Isotope Ratio Facility for Environmental Research (δ34S). We acknowledge permit numbers 00152-SCI-0020, 00196-SCI-0024, 00250-SCI-0023, 172-SCI-0021, and 00220-SCI-006 from the National Park Service, Gateway National Recreation Area, as well as New York State Department of Environmental Conservation permit number 81, issued to S. Elbin. This research was conducted under the approval of Cornell University's Institutional Animal Care and Use Committee (protocol 2001-0091). Support for this research was provided by the Berryman Institute, the Cornell University Biogeochemistry and Environmental Biocomplexity Program, the Garden Club of America, the Hudson River Foundation Polgar Fund, the Leon Levy Foundation, the Morris Animal Foundation, the National Oceanic and Atmospheric Administration, and the U.S. Department of Agriculture. We thank C. Weseloh and two anonymous reviewers for critical comments on an earlier draft of this manuscript.
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