Mercury contamination and stable isotopes reveal variability in foraging ecology of generalist California gulls
Graphical abstract
Introduction
Animals integrate unique signatures of habitat use, geography, and diet into body tissues from their prey, and therefore animal tissues can reveal elements of foraging ecology that can be unobtainable from direct observation or use of electronic tracking instruments (Ramos and González-Solís, 2012). Common ecological tracers used to study animal foraging ecology include light stable isotopes (e.g. C, N, H, and S) and fatty acids (Budge et al., 2006, Hobson, 1999, Inger and Bearhop, 2008, Peterson and Fry, 1987), and less commonly used tracers include environmental contaminants (Adams and Paperno, 2012, Calambokidis and Barlow, 1991, Catry et al., 2008). Contaminants, such as heavy metals and persistent organic pollutants, are often studied because of their potential impact on organism and ecosystem health (Tanabe, 2002, Wiener et al., 2003). However, some contaminants bioaccumulate in organisms and biomagnify in upper trophic level predators, which can allow these contaminants to serve as an ecological tracer and reveal elements of animal foraging ecology such as habitat type or location. Contaminants such as heavy metals and persistent organic pollutants are often non-uniformly distributed in the environment (Chasar et al., 2009, Meijer et al., 2003, Roscales et al., 2010), which may enable them to be used as tracers of habitat use at a regional or local scale.
Mercury (Hg) contamination in particular has many characteristics that may make it a useful ecological tracer. The unique processes that control methylmercury (MeHg) production from inorganic Hg are highly localized and vary substantially among habitat types (Eagles-Smith et al., 2016, Marvin-DiPasquale et al., 2003). As such, the biogeochemical processes influencing MeHg bioavailability in the environment can result in high variability in MeHg concentrations across aquatic and terrestrial habitats (Ullrich et al., 2001). Localized production of MeHg directly influences MeHg bioaccumulation in upper-trophic level predators because MeHg is the form of Hg that bioaccumulates in organisms and biomagnifies with increasing trophic level (Ullrich et al., 2001). Consequently, different habitat types in close proximity can contain markedly different MeHg concentrations in similar organisms (Chen et al., 2005, Eagles-Smith and Ackerman, 2014). For example, fish and bird MeHg concentrations varied up to 4-fold and 11-fold, respectively, in adjacent wetlands with different biogeochemistry (Ackerman et al., 2014a, Eagles-Smith and Ackerman, 2014). Additionally, MeHg concentrations can vary among similar habitats but geographically disjunct sites based on the availability of MeHg at the base of the food web and localized bioaccumulation processes (Evers et al., 2011, Scudder et al., 2009). Furthermore, as a result of biogeochemical processes and differences between aquatic and terrestrial food webs, MeHg concentrations often are much higher in animals deriving their diet from aquatic, rather than terrestrial, habitats (Ackerman et al., 2016b, McGrew et al., 2014, Ochoa-Acuña et al., 2002, Post, 2002).
MeHg and stable isotopes in consumer tissues represent an integrated diet over varying lengths of time, depending on the tissue (Lewis and Furness, 1991, Vander Zanden et al., 2015, Wang et al., 2014), and variability in these tracers can reveal different components of animal foraging ecology (Caron-Beaudoin et al., 2013, Moreno et al., 2010, Ramos et al., 2009). Trophic position within a habitat can be established using δ15N values and MeHg concentrations (Anderson et al., 2009, Campbell et al., 2005). Habitat type and sources of primary productivity to a food web can be discriminated using carbon isotope ratios, although δ13C values also increase with trophic level but to a lesser degree than δ15N values (Inger and Bearhop, 2008, Peterson and Fry, 1987). Sulfur isotope ratios, considered to have low or undetectable levels of fractionation with trophic position, have been effectively used to reveal habitat use along a terrestrial to marine gradient for multiple taxonomic groups (Barros et al., 2010, Cotin et al., 2011, Fry and Chumchal, 2011, Lott et al., 2003, Ramos et al., 2009, Zazzo et al., 2011). MeHg concentrations can also relate to habitat use along a terrestrial to marine gradient, likely as a result of sulfate reduction and increased methylation in specific habitat types (Gabriel et al., 2014, Gilmour et al., 1992). Moreover, MeHg concentrations in organisms may reveal additional aspects of an animal’s foraging ecology, including separation of foraging locations or specific habitats, than traditional ecological tracers (Adams and Paperno, 2012, Catry et al., 2008). For example, in a study where stable isotopes were inconclusive in differentiating foraging ecology of tropical seabirds, the addition of MeHg resulted in the ability to differentiate foraging locations (Catry et al., 2008). Therefore, MeHg may be a useful tracer to differentiate diet and foraging strategies for generalist species that forage across a range of diverse habitats, and complement traditional ecological tracers like light stable isotopes.
We used a combination of total Hg (THg) concentrations and light stable isotopes (nitrogen, carbon, and sulfur) of a generalist predator, the California gull (Larus californicus), to examine variability in foraging strategies and to illustrate the utility of using Hg contamination as an ecological tracer of foraging ecology. While in the San Francisco Bay Estuary (California, USA), California gulls can access marine and estuarine prey resources, as well as terrestrial anthropogenic diet sources associated with several large landfills along the bay margins. We used a traditional approach of using light stable isotopes to identify clusters of birds with similar foraging ecology during the pre-breeding and breeding time periods, and then examined if foraging clusters of gulls could be differentiated based upon their Hg contamination. We hypothesized that gulls from different foraging clusters would vary in their use of terrestrially-derived prey (from landfills), and that gulls with higher proportions of diet derived from landfills would result in lower Hg contamination than gulls with a higher proportion of diet derived from aquatic, estuarine prey. Additionally, because sulfur isotopes are strongly reflective of foraging along a terrestrial to marine gradient, we examined whether δ34S values directly related to THg concentrations to demonstrate if Hg concentrations could link to animal foraging ecology.
Section snippets
Sample collection
We captured adult California gulls in 2007 and 2008 using rocket nets (Dill and Thornsberry, 1950), remotely detonated net launchers (Coda Enterprises, Mesa, Arizona, USA), and bow nets at three breeding colonies in south San Francisco Bay, California, USA (A6, Coyote Hills, and Mowry colonies; Ackerman et al., 2014b) from 6-March to 26-April, prior to the breeding season, and from 15-May to 30-May, during the breeding season. We captured chicks by hand from 16-June to 3-July, late in the
Foraging ecology clustered by isotopes
California gull adults and chicks clustered into multiple foraging strategies, using δ34S, δ15N, and δ13C values. We observed high variability among adult California gulls (n = 146) for stable isotope values between and within seasons, with pre-breeding birds (δ34S: −2.6 to 19.2‰; δ15N: 6.9 to 18.4‰; δ13C: −20.5 to −15.7‰) having a wider range of stable isotope values than breeding birds (δ34S: 2.6–7.6‰; δ15N: 8.0–12.6‰; δ13C: −19.7 to −16.2‰; Table A1). Pre-breeding California gulls grouped into
Discussion
Environmental contaminants are rarely used as ecological tracers, but some contaminants vary substantially among habitats, particularly those like Hg whose biological availability is dependent on the presence of certain biogeochemical processes (Marvin-DiPasquale et al., 2003). Biogeochemical processes that convert relatively biologically unavailable inorganic Hg to highly bioaccumulative MeHg and allow MeHg to biomagnify through food webs can make this contaminant particularly useful for
Acknowledgments
This research was funded by the State Coastal Conservancy, South Bay Salt Pond Restoration Project, U.S. Fish and Wildlife Service Coastal Program in San Francisco Bay, and U.S. Geological Survey Western Ecological Research Center. We thank Cheryl Strong, Eric Mruz, Clyde Morris, Joy Albertson, Joelle Buffa, Mendel Stewart, Marge Kolar, Tom Maurer, Carol Atkins, the staff at the Don Edwards San Francisco Bay National Wildlife Refuge, San Francisco Bay Bird Observatory, the U.S. Fish and
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