Changing gull diet in a changing world: A 150‐year stable isotope (δ13C, δ15N) record from feathers collected in the Pacific Northwest of North America
TL;DR: Stable isotope analysis of feathers from glaucous-winged gulls in a heavily disturbed region of the northeast Pacific suggests a long-term decrease in diet quality linked to declining fish abundance or other anthropogenic influences, and may help to explain regional population declines in this species and other piscivores.
Abstract: The world's oceans have undergone significant ecological changes following European colonial expansion and associated industrialization. Seabirds are useful indicators of marine food web structure and can be used to track multidecadal environmental change, potentially reflecting long-term human impacts. We used stable isotope (δ(13)C, δ(15)N) analysis of feathers from glaucous-winged gulls (Larus glaucescens) in a heavily disturbed region of the northeast Pacific to ask whether diets of this generalist forager changed in response to shifts in food availability over 150 years, and whether any detected change might explain long-term trends in gull abundance. Sampled feathers came from birds collected between 1860 and 2009 at nesting colonies in the Salish Sea, a transboundary marine system adjacent to Washington, USA and British Columbia, Canada. To determine whether temporal trends in stable isotope ratios might simply reflect changes to baseline environmental values, we also analysed muscle tissue from forage fishes collected in the same region over a multidecadal timeframe. Values of δ(13)C and δ(15)N declined since 1860 in both subadult and adult gulls (δ(13)C, ~ 2-6‰; δ(15)N, ~4-5‰), indicating that their diet has become less marine over time, and that birds now feed at a lower trophic level than previously. Conversely, forage fish δ(13)C and δ(15)N values showed no trends, supporting our conclusion that gull feather values were indicative of declines in marine food availability rather than of baseline environmental change. Gradual declines in feather isotope values are consistent with trends predicted had gulls consumed less fish over time, but were equivocal with respect to whether gulls had switched to a more garbage-based diet, or one comprising marine invertebrates. Nevertheless, our results suggest a long-term decrease in diet quality linked to declining fish abundance or other anthropogenic influences, and may help to explain regional population declines in this species and other piscivores.
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TL;DR: This study demonstrates the overall conservatism of the finch gut microbiome over short (< 1 Ma) divergence timescales, except in the most extreme case of dietary specialization, and elevates the evolutionary importance of seasonal shifts in driving not only species adaptation, but also gut microbiome composition.
Abstract: Darwin’s finches are a clade of 19 species of passerine birds native to the Galapagos Islands, whose biogeography, specialized beak morphologies, and dietary choices—ranging from seeds to blood—make them a classic example of adaptive radiation While these iconic birds have been intensely studied, the composition of their gut microbiome and the factors influencing it, including host species, diet, and biogeography, has not yet been explored We characterized the microbial community associated with 12 species of Darwin’s finches using high-throughput 16S rRNA sequencing of fecal samples from 114 individuals across nine islands, including the unusual blood-feeding vampire finch (Geospiza septentrionalis) from Darwin and Wolf Islands The phylum-level core gut microbiome for Darwin’s finches included the Firmicutes, Gammaproteobacteria, and Actinobacteria, with members of the Bacteroidetes at conspicuously low abundance The gut microbiome was surprisingly well conserved across the diversity of finch species, with one exception—the vampire finch—which harbored bacteria that were either absent or extremely rare in other finches, including Fusobacterium, Cetobacterium, Ureaplasma, Mucispirillum, Campylobacter, and various members of the Clostridia—bacteria known from the guts of carnivorous birds and reptiles Complementary stable isotope analysis of feathers revealed exceptionally high δ15N isotope values in the vampire finch, resembling top marine predators The Galapagos archipelago is also known for extreme wet and dry seasons, and we observed a significant seasonal shift in the gut microbial community of five additional finch species sampled during both seasons This study demonstrates the overall conservatism of the finch gut microbiome over short (< 1 Ma) divergence timescales, except in the most extreme case of dietary specialization, and elevates the evolutionary importance of seasonal shifts in driving not only species adaptation, but also gut microbiome composition
58 citations
TL;DR: High prevalence of terrestrial foraging during early breeding as well as support for dietary switching early in the breeding season are found, suggesting anthropogenic terrestrial food sources may play a role in the low breeding success of these gulls through either variation in quantity and/or quality.
Abstract: Generalist predators may vary their diet and use of habitat according to both internal state (e.g. breeding stage) and external (e.g. weather) factors. Lesser black-backed gulls Larus fuscus (Linnaeus 1758) are dietary generalists, foraging in both terrestrial and marine habitats during breeding. We investigate what affects the gulls’ propensity to forage at sea or on land. We assess the importance of terrestrial foraging to gulls in the Baltic Sea (sub. sp. L. f. fuscus), looking especially at their use of agricultural fields. Through the GPS tracking of 19 individuals across 3 years we tracked 1038 foraging trips and found that 21.2 % of foraging trips were predominantly terrestrial, 9.0 % were a mix of terrestrial and marine, and 68.5 % were exclusively marine. Terrestrial trips were (1) more frequent when departing around sunrise, whereas marine trips occurred throughout the day. Additionally, trips with mostly land-based foraging decreased as the breeding season progressed, suggesting dietary switching coincident with the onset of chick provisioning. (2) During cloudy and cold conditions terrestrial foraging trips were more likely. (3) We found no differences between sexes in their land-based foraging strategy. (4) Gull individuals showed great variation in foraging strategy. Using observations of agricultural fields, carried out for one year, we found that (5) gulls preferentially foraged on fields with short vegetation, and there was a positive association with occurrence of waders and other species of gulls. (6) The availability and use of these preferred fields decreased through the breeding period. This study found high prevalence of terrestrial foraging during early breeding as well as support for dietary switching early in the breeding season. The overall tendency for marine or terrestrial foraging was consistent within individuals, with gull identity accounting for much of the variation observed in foraging trips. Our results suggest that anthropogenic terrestrial food sources may play a role in the low breeding success of these gulls through either variation in quantity and/or quality. Finally, our study demonstrates the potential of combining data from GPS-tracking of individual animals with the ‘ground-truthing’ of habitat visited to elucidate the otherwise nebulous behavior of a generalist predator.
57 citations
Cites background from "Changing gull diet in a changing wo..."
...Stable isotope analysis of feathers from gulls in one area taken over several decades suggested increasing reliance on terrestrial food sources likely due to declining fish abundance [16]....
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TL;DR: Results are consistent with the hypothesis that aerial insectivore populations are declining due to changes in abundance of higher trophic-level prey, but it is cautioned that museum-based stable isotope studies of terrestrial food chains will require new approaches to assessing baseline change.
Abstract: Identifying the mechanisms of ecological change is challenging in the absence of long-term data, but stable isotope ratios of museum specimen tissues may provide a record of diet and habitat change through time. Aerial insectivores are experiencing the steepest population declines of any avian guild in North America and one hypothesis for these population declines is a reduction in the availability of prey. If reduced prey availability is due to an overall reduction in insect abundance, we might also expect populations of higher trophic level insects to have declined most quickly due to their greater sensitivity to a variety of disturbance types. Because nitrogen isotope ratios (delta 15N) tend to increase with trophic-level, while delta 13C generally increases with agricultural intensification, we used delta 15N and 13C values of bird tissues grown in winter (claw) and during breeding (feathers) from museum specimens spanning 1880–2005, and contemporary samples from breeding birds (2011–2013) to test for diet change in a migratory nocturnal aerial insectivore, Eastern Whip-poor-will (Antrostomus vociferus) breeding in Ontario, Canada. To test if environmental baselines have changed as a result of synthetic N fertilizer use, habitat conversion or climate, we also sampled delta 15N values of three potential prey species collected from across the same geographic region and time period. Over the past 100 years, we found a significant decline in delta 15N in tissues grown on both the breeding and wintering grounds. Prey species did not show a corresponding temporal trend in delta 15N values, but our power to detect such a trend was limited due to higher sample variance. Amongst contemporary bird samples, delta 15N values did not vary with sex or breeding site, but nestlings had lower values than adults. These results are consistent with the hypothesis that aerial insectivore populations are declining due to changes in abundance of higher trophic-level prey, but we caution that museum-based stable isotope studies of terrestrial food chains will require new approaches to assessing baseline change. Once addressed, an ability to decode the historical record locked inside museum collections could enhance our understanding of ecological change and inform conservation decisions.
46 citations
TL;DR: Variation in Hg in seabirds across space and time was associated with the origin of sulfur in the diet, and variation within and among seab birds near the top of the food web was associatedwith variation in δ34S at the base of theFood web more so than trophic position within the foodweb.
Abstract: Mercury (Hg) is a neurotoxin that can be particularly harmful to top predators because it biomagnifies through the food web. Due to variation in the food web structure, variation in Hg exposure in predators may represent variation in diet rather than Hg availability. We measured Hg in eggs from six seabird species (N = 537) over 47 years. In contrast to expectation, storm-petrels feeding partially on invertebrates had the highest Hg burden while herons feeding on large fish had the lowest Hg burden. A multiple regression showed that Hg correlated with δ34S (R2 = 0.86) rather than trophic level (δ15N of “trophic” amino acids). Sulfate-rich environments (high δ34S) have sulfate-reducing bacteria that produce methylmercury. Variation in Hg within and among seabirds near the top of the food web was associated with variation in δ34S at the base of the food web more so than trophic position within the food web. Hg levels in seabirds only changed over time for those species where δ34S also varied in tandem; afte...
44 citations
TL;DR: This work synthesise and critically evaluate a total of 18 studies covering eight avian species published between 2008 and 2018 across four continents that report flame retardant (FR) burdens in birds utilising landfill, and recommends that ongoing research be focused on landfill-associated birds.
39 citations
References
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State Street Corporation1, University of California, Santa Barbara2, University of Hawaii at Manoa3, Stanford University4, Arizona State University5, Wildlife Conservation Society6, University of North Carolina at Chapel Hill7, National Oceanic and Atmospheric Administration8, Environmental Defense Fund9, Ocean Conservancy10, The Nature Conservancy11, University of Maine12, University of British Columbia13
TL;DR: This article developed an ecosystem-specific, multiscale spatial model to synthesize 17 global data sets of anthropogenic drivers of ecological change for 20 marine ecosystems and found that no area is unaffected by human influence and that a large fraction (41%) is strongly affected by multiple drivers.
Abstract: The management and conservation of the world's oceans require synthesis of spatial data on the distribution and intensity of human activities and the overlap of their impacts on marine ecosystems. We developed an ecosystem-specific, multiscale spatial model to synthesize 17 global data sets of anthropogenic drivers of ecological change for 20 marine ecosystems. Our analysis indicates that no area is unaffected by human influence and that a large fraction (41%) is strongly affected by multiple drivers. However, large areas of relatively little human impact remain, particularly near the poles. The analytical process and resulting maps provide flexible tools for regional and global efforts to allocate conservation resources; to implement ecosystem-based management; and to inform marine spatial planning, education, and basic research.
5,365 citations
University of California, Santa Cruz1, Duke University2, University of California, Berkeley3, University of Montana4, University of Cape Town5, University of Wisconsin-Madison6, University of Washington7, University of Florida8, Scripps Institution of Oceanography9, University of Missouri–St. Louis10, Finnmark University College11, University of Turku12, Stony Brook University13, Oregon State University14, Wageningen University and Research Centre15, University of California, Davis16, University of British Columbia17, University of Oulu18, Swedish University of Agricultural Sciences19
TL;DR: This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles.
Abstract: Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these animals may be humankind's most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.
3,130 citations
"Changing gull diet in a changing wo..." refers background in this paper
...The profound and potentially irreversible ecological consequences of such changes (Estes et al., 2011) make it important to improve our understanding of them, particularly given their widespread nature and the growing public concern over ocean health (Crain et al., 2009)....
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...The profound and potentially irreversible ecological consequences of such changes (Estes et al., 2011) make it important to improve our understanding of them, particularly given their widespread nature and the growing public concern over ocean health (Crain et al....
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TL;DR: The results indicate that lipid extraction or normalization is most important when lipid content is variable among consumers of interest or between consumers and end members, and when differences in δ13C between end members is <10–12‰.
Abstract: Within an organism, lipids are depleted in (13)C relative to proteins and carbohydrates (more negative delta(13)C), and variation in lipid content among organisms or among tissue types has the potential to introduce considerable bias into stable isotope analyses that use delta(13)C. Despite the potential for introduced error, there is no consensus on the need to account for lipids in stable isotope analyses. Here we address two questions: (1) If and when is it important to account for the effects of variation in lipid content on delta(13)C? (2) If it is important, which method(s) are reliable and robust for dealing with lipid variation? We evaluated the reliability of direct chemical extraction, which physically removes lipids from samples, and mathematical normalization, which uses the carbon-to-nitrogen (C:N) ratio of a sample to normalize delta(13)C after analysis by measuring the lipid content, the C:N ratio, and the effect of lipid content on delta(13)C (Deltadelta(13)C) of plants and animals with a wide range of lipid contents. For animals, we found strong relationships between C:N and lipid content, between lipid content and Deltadelta(13)C, and between C:N and Deltadelta(13)C. For plants, C:N was not a good predictor of lipid content or Deltadelta(13)C, but we found a strong relationship between carbon content and lipid content, lipid content and Deltadelta(13)C, and between and carbon content and Deltadelta(13)C. Our results indicate that lipid extraction or normalization is most important when lipid content is variable among consumers of interest or between consumers and end members, and when differences in delta(13)C between end members is <10-12 per thousand. The vast majority of studies using natural variation in delta(13)C fall within these criteria. Both direct lipid extraction and mathematical normalization reduce biases in delta(13)C, but mathematical normalization simplifies sample preparation and better preserves the integrity of samples for delta(15)N analysis.
2,103 citations
"Changing gull diet in a changing wo..." refers background or methods in this paper
...Based on their C : N ratios, mean lipid levels of our sampled eulachon were in excess of 33% (cf. Post et al., 2007)....
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...4 SD) were high enough to indicate an elevated tissue lipid content and resulting biased estimates of δ(13)C values (Post et al., 2007); thus, we excluded eulachon data from analyses of δ(13)C trends in fish (i....
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...C : N ratios for eulachon samples (mean 7.8 2.4 SD) were high enough to indicate an elevated tissue lipid content and resulting biased estimates of d13C values (Post et al., 2007); thus, we excluded eulachon data from analyses of d13C trends in fish (i.e., our proxy for environmental change)....
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...C : N ratios of herring and sandlance were relatively low (3.4–4.4), so we assumed no effect of lipid content on reported d13C values for these two species, again following Post et al. (2007)....
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...Instead, following Post et al. (2007), we used C : N ratios of analysed samples to assess lipid content....
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TL;DR: This paper reviews the use of stable isotope analyses to trace nutritional origin and migration in animals and concludes that this technique will be extremely useful in helping to track migration and movement of a wide range of animals from insects to birds and mammals.
Abstract: To understand the ecology of migratory animals it is important to link geographic regions used by individuals including breeding, wintering, and intermediate stopover sites. Previous conventional approaches used to track animal movements have relied on extrinsic markers and typically the subsequent recovery of individuals. This approach has generally been inappropriate for most small, or non-game animals. The use of intrinsic markers such as fatty acid profiles, molecular DNA analyses, and the measurement of naturally occurring stable isotopes in animal tissues offer alternative approaches. This paper reviews the use of stable isotope analyses (primarily δ13C, δ15N, δ34S, δD, δ87Sr) to trace nutritional origin and migration in animals. This approach relies on the fact that foodweb isotopic signatures are reflected in the tissues of organisms and that such signatures can vary spatially based on a variety of biogeochemical processes. Organisms moving between isotopically distinct foodwebs can carry with them information on the location of previous feeding. Such an approach has been used to track animal use of inshore versus offshore, marine versus freshwater, terrestrial C3 versus marine, terrestrial mesic versus xeric, and C3 versus C4 or Crassulacean acid metabolism foodwebs. More recently, the use of stable hydrogen isotope analyses (δD) to link organisms to broad geographic origin in North America is based on large-scale isotopic contours of growing-season average δD values in precipitation. This technique, especially when combined with the assay of other stable isotopes, will be extremely useful in helping to track migration and movement of a wide range of animals from insects to birds and mammals. Future research to refine our understanding of natural and anthropogenic-induced isotopic gradients in nature, and to explore the use of stable isotopes of other elements, is recommended.
1,628 citations
"Changing gull diet in a changing wo..." refers background in this paper
...Once grown, feathers are metabolically inert, so their isotopic values reflect diet during the period of feather generation (Mizutani et al., 1990; Hobson, 1999)....
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Book•
01 Jan 2006TL;DR: The omnivor's dilemma: a natural history of four meals , The omnivore's dilemma): a naturalHistory of three meals, and more.
Abstract: The omnivore's dilemma: a natural history of four meals , The omnivore's dilemma: a natural history of four meals , مرکز فناوری اطلاعات و اطلاع رسانی کشاورزی
1,218 citations
"Changing gull diet in a changing wo..." refers background in this paper
...About 98% of our feather samples were either from birds at Canadian colonies, or from the United States but collected prior to the 1950s, when corn was widely adopted as feed for poultry and cattle (Pollan 2006)....
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...About 98% of our feather samples were either from birds at Canadian colonies, or from the United States but collected prior to the 1950s, when corn was widely adopted as feed for poultry and cattle (Pollan 2006)....
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