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.

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.

Tracking overwintering areas of fish-eating birds to identify mercury exposure.

Migration patterns are believed to greatly influence concentrations of contaminants in birds due to accumulation in spatially and temporally distinct ecosystems. Two species of fish-eating birds, the Double-crested Cormorant (Phalacrocorax auritus) and the Caspian Tern (Hydroprogne caspia) breeding in Lake Ontario were chosen to measure the impact of overwintering location on mercury concentrations ([Hg]). We characterized (1) overwintering areas using stable isotopes of hydrogen (δ(2)H) and band recoveries, and (2) overwintering habitats by combining information from stable isotopes of sulfur (δ(34)S), carbon (δ(13)C), nitrogen (δ(15)N), and δ(2)H in feathers grown during the winter. Overall, overwintering location had a significant effect on [Hg]. Both species showed high [Hg] in (13)C-rich habitats. In situ production of Hg (e.g., through sulfate reducing bacteria in sediments) and allochthonous import could explain high [Hg] in birds visiting (13)C-rich habitats. Higher [Hg] were found in birds with high δ(2)H, suggesting that Hg is more bioavailable in southern overwintering locations. Hotspot maps informed that higher [Hg] in birds were found at the limit of their southeastern overwintering range. Mercury concentrations in winter feathers were positively related to predicted spatial pattern of [Hg] in fish using the National Descriptive Model of Mercury in Fish (NDMMF) based on bird spatial assignment (using δ(2)H). This study indicates that the overwintering location greatly influences [Hg].

Contamination of mercury during the wintering period influences concentrations at breeding sites in two migratory piscivorous birds.

Many aquatic fish-eating birds migrate long distances and are exposed to different mercury concentrations ([Hg]) during their annual cycle. Here we examined the importance of migration on [Hg] in two colonial migratory fish-eating bird species. We determined temporal trends of [Hg] and stable isotopes of carbon (δ(13)C) and nitrogen (δ(15)N) during the annual cycle in Double-crested Cormorants (Phalacrocorax auritus) and Caspian Terns (Hydroprogne caspia) breeding in Lake Ontario by a repeated sampling of breast feathers and blood from recaptured individuals. We found an effect of previous winter [Hg], species, sex, and location to explain variations of Hg at breeding sites. This suggests Hg carryover from winter to summer periods and that variations of [Hg] in the summer are partially explained by [Hg] in the winter. Carryover of Hg among seasons and slow changes in [Hg] over time were found especially for individuals in high winter exposure groups, suggesting a slow depuration rate and a fast uptake rate for both species. In contrast, stable isotope values rapidly switched to reach equilibrium at a similar midpoint regardless of winter habitat or diet suggesting minimal carryover of isotopic signatures. The potential of Hg carryover from wintering sites indicates that Hg concentrations in birds at a given time may be influenced by previous exposure from distant locations.

Natal dispersal driven by environmental conditions interacting across the annual cycle of a migratory songbird.

Natal dispersal, the process through which immature individuals permanently depart their natal area in search of new sites, is integral to the ecology and evolution of animals. Insights about the underlying causes of natal dispersal arise mainly from research on species whose short dispersal distances or restricted distributions make them relatively easy to track. However, for small migratory animals, the causes of natal dispersal remain poorly understood because individuals are nearly impossible to track by using conventional mark-recapture approaches. Using stable-hydrogen isotope ratios in feathers of American redstarts (Setophaga ruticilla) captured as immature birds and again as adults, we show that habitat use during the first tropical nonbreeding season appears to interact with latitudinal gradients in spring phenology on the temperate breeding grounds to influence the distance traveled on the initial spring migration and the direction of natal dispersal. In contrast, adult redstarts showed considerable site fidelity between breeding seasons, indicating that environmental conditions did not affect dispersal patterns after the first breeding attempt. Our findings suggest that habitat occupancy during the first nonbreeding season helps determine the latitude at which this species of Neotropical-Nearctic migratory bird breeds throughout its life and emphasize the need to understand how events throughout the annual cycle interact to shape fundamental biological processes.

Early-Life Corticosterone Body Condition Influence Social Status and Survival in a Food-Caching Passerine.

Individuals undergo profound changes throughout their early life as they grow and transition between life-history stages. As a result, the conditions that individuals experience during development can have both immediate and lasting effects on their physiology, behavior, and, ultimately, fitness. In a population of Canada jays in Algonquin Provincial Park, Ontario, Canada, we characterized the diet composition and physiological profile of young jays at three key time points during development (nestling, pre-fledge, and pre-dispersal) by quantifying stable-carbon (δ13C) and -nitrogen (δ15N) isotopes and corticosterone concentrations in feathers. We then investigated the downstream effects of early-life diet composition, feather corticosterone, and environmental conditions on a juvenile's social status, body condition, and probability of being observed in the fall following hatch. Across the three time points, the diet of Canada jay young was composed primarily of vertebrate tissue and human food with the proportion of these food items increasing as the jays neared dispersal. Feather corticosterone concentrations also shifted across the three time points, decreasing from nestling to pre-dispersal. Dominant juveniles had elevated corticosterone concentrations in their feathers grown pre-dispersal compared with subordinates. High body condition as nestlings was associated with high body condition as juveniles and an increased probability of being observed in the fall. Together, our results demonstrate that nestling physiology and body condition influence the social status and body condition once individuals are independent, with potential long-term consequences on survival and fitness.

Postprandial zinc stable isotope response in human blood serum.

In recent years, considerable advances have been made in the field of medical isotope metallomics, but numerous fundamental physiological processes remain to be investigated. Past studies report that blood serum Zn concentrations decrease by between about 10 and 25%, depending on the size of meal, approximately three hours postprandially (i.e. after eating), before returning to baseline values if no meals are consumed over the following four to five hours. Nine participants were recruited for this study to investigate whether this postprandial Zn concentration decrease is accompanied by a stable isotope response. A baseline serum sample was collected from participants in the morning after overnight fasting. A 576 kcal meal was then provided and additional serum samples were taken 90 and 180 minutes post-meal to coincide with the postprandial response. Serum Zn concentrations decreased postprandially by an average of 21 ± 9% (1SD), but this was not accompanied by a change in stable Zn isotope composition (mean Δ66Zn180-minute-baseline = 0.01 ± 0.09‰, 2SD). We propose that hemodilution and the rapid, efficient postprandial transfer of albumin-bound Zn from serum to the liver and pancreas is responsible for the lack of postprandial serum Zn isotopic response. These results indicate that studies examining solely the distribution of Zn isotopes in serum may obtain samples without considering timing of the most recent meal. However, future studies seeking to compare serum Zn concentrations with δ66Zn values should draw blood samples in the morning after overnight fasting.

Non-breeding season events influence sexual selection in a long-distance migratory bird.

The study of sexual selection has traditionally focused on events and behaviours immediately surrounding copulation. In this study, we examine whether carry-over effects from the non-breeding season can influence the process of sexual selection in a long-distance migratory bird, the American redstart (Setophaga ruticilla). Previous work on American redstarts demonstrated that overwintering in a high-quality habitat influences spring departure dates from the wintering grounds, advances arrival dates on the breeding grounds and increases apparent reproductive success. We show that the mixed-mating strategy of American redstarts compounds the benefits of overwintering in high-quality winter habitats. Males arriving to breed in Canada from high-quality winter habitats arrive earlier than males from poor-quality habitats, resulting in a lower probability of paternity loss, a higher probability of achieving polygyny and ultimately higher realized reproductive success. Such results suggest that the process of sexual selection may be influenced by events interacting throughout the annual cycle.

Carry-over effects in a Pacific seabird: stable isotope evidence that pre-breeding diet quality influences reproductive success.

1. Understanding the interactions between different periods of the annual cycle in migratory animals has been constrained by our inability to track individuals across seasons. In seabirds, virtually nothing is known about how diet quality during the non-breeding period, away from the breeding grounds, might influence subsequent reproductive success. 2. We used stable nitrogen (delta(15)N) and carbon (delta(13)C) isotopes to evaluate the effects of non-breeding diet quality on the timing of breeding and egg size in a population of Cassin's auklets (Ptychoramphus aleuticus) breeding on Triangle Island, British Columbia. Adult feathers are grown during two different periods of the annual cycle, which allowed us to estimate diet quality from the previous fall (October-November) and pre-breeding (February-March) period. 3. We found that the estimated proportion of energetically superior copepods (Neocalanus spp.) in the pre-breeding diet tended to be higher in females that bred earlier and laid larger eggs, whereas energetically poor juvenile rockfish (Sebastes spp.) were dominant in the pre-breeding diets of females that bred later and laid smaller eggs. We detected no effect of fall diet quality on breeding date or egg size, and no effect of pre-breeding diet quality on breeding date in males. 4. Pre-breeding diet quality was not related to body condition measured 1-2 days after laying, which suggests that females may need to attain a threshold condition before they initiate breeding and successfully rear young. 5. Our results suggest that changes in climatic conditions during the pre-breeding period may have severe consequences for reproductive success by influencing breeding date and egg size. Our work emphasizes the importance of determining how events are linked throughout the annual cycle for understanding the fitness and population dynamics of migratory animals.

Stable isotopes can be used to infer the overwintering locations of prebreeding marine birds in the Canadian Arctic.

Although assessments of winter carryover effects on fitness-related breeding parameters are vital for determining the links between environmental variation and fitness, direct methods of determining overwintering distributions (e.g., electronic tracking) can be expensive, limiting the number of individuals studied. Alternatively, stable isotope analysis in specific tissues can be used as an indirect means of determining individual overwintering areas of residency. Although increasingly used to infer the overwintering distributions of terrestrial birds, stable isotopes have been used less often to infer overwintering areas of marine birds. Using Arctic-breeding common eiders, we test the effectiveness of an integrated stable isotope approach (13-carbon, 15-nitrogen, and 2-hydrogen) to infer overwintering locations. Knowing the overwinter destinations of eiders from tracking studies at our study colony at East Bay Island, Nunavut, we sampled claw and blood tissues at two known overwintering locations, Nuuk, Greenland, and Newfoundland, Canada. These two locations yielded distinct tissue-specific isotopic profiles. We then compared the isotope profiles of tissues collected from eiders upon their arrival at our breeding colony, and used a k-means cluster analysis approach to match arriving eiders to an overwintering group. Samples from the claws of eiders were most effective for determining overwinter origin, due to this tissue's slow growth rate relative to the 40-day turnover rate of blood. Despite taking an integrative approach using multiple isotopes, k-means cluster analysis was most effective when using 13-carbon alone to assign eiders to an overwintering group. Our research demonstrates that it is possible to use stable isotope analysis to assign an overwintering location to a marine bird. There are few examples of the effective use of this technique on a marine bird at this scale; we provide a framework for applying this technique to detect changes in the migration phenology of birds' responses to rapid changes in the Arctic.

Linking Isotopes and Panmixia: High Within-Colony Variation in Feather δ2H, δ13C, and δ15N across the Range of the American White Pelican.

Complete panmixia across the entire range of a species is a relatively rare phenomenon; however, this pattern may be found in species that have limited philopatry and frequent dispersal. American white pelicans (Pelecanus erythrorhyncos) provide a unique opportunity to examine the role of long-distance dispersal in facilitating gene flow in a species recently reported as panmictic across its broad breeding range. This species is also undergoing a range expansion, with new colonies arising hundreds of kilometers outside previous range boundaries. In this study, we use a multiple stable isotope (δ2H, δ13C, δ15N) approach to examine feather isotopic structuring at 19 pelican colonies across North America, with the goal of establishing an isotopic basemap that could be used for assigning individuals at newly established breeding sites to source colonies. Within-colony isotopic variation was extremely high, exceeding 100‰ in δ2H within some colonies (with relatively high variation also observed for δ13C and δ15N). The high degree of within-site variation greatly limited the utility of assignment-based approaches (42% cross-validation success rate; range: 0-90% success). Furthermore, clustering algorithms identified four likely isotopic clusters; however, those clusters were generally unrelated to geographic location. Taken together, the high degree of within-site isotopic variation and lack of geographically-defined isotopic clusters preclude the establishment of an isotopic basemap for American white pelicans, but may indicate that a high incidence of long-distance dispersal is facilitating gene flow, leading to genetic panmixia.

Experimental evidence shows no fractionation of strontium isotopes ((87)Sr/(86)Sr) among soil, plants, and herbivores: implications for tracking wildlife and forensic science.

Strontium isotopes ((87)Sr/(86)Sr) can be useful biological markers for a wide range of forensic science applications, including wildlife tracking. However, one of the main advantages of using (87)Sr/(86)Sr values, that there is no fractionation from geological bedrock sources through the food web, also happens to be a critical assumption that has never been tested experimentally. We test this assumption by measuring (87)Sr/(86)Sr values across three trophic levels in a controlled greenhouse experiment. Adult monarch butterflies were raised on obligate larval host milkweed plants that were, in turn, grown on seven different soil types collected across Canada. We found no significant differences between (87)Sr/(86)Sr values in leachable Sr from soil minerals, organic soil, milkweed leaves, and monarch butterfly wings. Our results suggest that strontium isoscapes developed from (87)Sr/(86)Sr values in bedrock or soil may serve as a reliable biological marker in forensic science for a range of taxa and across large geographic areas.

Tropical winter habitat limits reproductive success on the temperate breeding grounds in a migratory bird.

Identifying the factors that control population dynamics in migratory animals has been constrained by our inability to track individuals throughout the annual cycle. Using stable carbon isotopes, we show that the reproductive success of a long-distance migratory bird is influenced by the quality of habitat located thousands of kilometres away on tropical wintering grounds. For male American redstarts (Setophaga ruticilla), winter habitat quality influenced arrival date on the breeding grounds, which in turn affected key variables associated with reproduction, including the number of young fledged. Based on a winter-habitat model, females occupying high-quality winter habitat were predicted to produce more than two additional young and to fledge offspring up to a month earlier compared with females wintering in poor-quality habitat. Differences of this magnitude are highly important considering redstarts are single brooded, lay clutches of only three to five eggs and spend only two-and-a-half months on the breeding grounds. Results from this study indicate the importance of understanding how periods of the annual cycle interact for migratory animals. Continued loss of tropical wintering habitat could have negative effects on migratory populations in the following breeding season, minimizing density-dependent effects on the breeding grounds and leading to further population declines. If conservation efforts are to be successful, strategies must incorporate measures to protect all the habitats used during the entire annual cycle of migratory animals.

The long and the short of it: no dietary specialisation between male and female western sandpipers despite strong bill size dimorphism.

Many bird species show spatial or habitat segregation of the sexes during the non-breeding season. One potential ecological explanation is that differences in bill morphology favour foraging niche specialisation and segregation. Western sandpipers Calidris mauri have pronounced bill size dimorphism, with female bills averaging 15% longer than those of males. The sexes differ in foraging behaviour and exhibit partial latitudinal segregation during the non-breeding season, with males predominant in the north and females in the south. Niche specialisation at a local scale might account for this broad geographic pattern, and we investigated whether longer-billed females and shorter-billed males occupy different foraging niches at 16 sites across the non-breeding range. We used stable-nitrogen (δ(15)N) isotope analysis of whole blood to test for dietary specialisation according to bill length and sex. Stable-nitrogen isotope ratios increase with trophic level. We predicted that δ(15)N values would increase with bill length and would be higher for females, which use a greater proportion of foraging behaviour that targets higher-trophic level prey. We used stable-carbon (δ(13)C) isotope analysis to test for habitat segregation according to bill length and sex. Stable-carbon isotope ratios vary between marine- and freshwater-influenced habitats. We predicted that δ(13)C values would differ between males and females if the sexes segregate between habitat types. Using a model selection approach, we found little support for a relationship between δ(15)N and either bill length or sex. There was some indication, however, that more marine δ(13)C values occur with shorter bill lengths. Our findings provide little evidence that male and female western sandpipers exhibit dietary specialisation as a function of their bill size, but indicate that the sexes may segregate in different habitats according to bill length at some non-breeding sites. Potential ecological factors underlying habitat segregation between sexes include differences in preferred habitat type and predation risk.

Herbivory in a spider through exploitation of an ant-plant mutualism.

Spiders are thought to be strict predators. We describe a novel exception: Bagheera kiplingi, a Neotropical jumping spider (Salticidae) that exploits a well-studied ant-plant mutualism, is predominantly herbivorous. From behavioral field observations and stable-isotope analyses, we show that the main diet of this host-specific spider comprises specialized leaf tips (Beltian food bodies; Figure 1A) from Vachellia spp. ant-acacias (formerly Acacia spp.), structures traded for protection in the plant's coevolved mutualism with Pseudomyrmex spp. ants that inhabit its hollow thorns. This is the first report of a spider that feeds primarily and deliberately on plants.

Geographic variation of strontium and hydrogen isotopes in avian tissue: implications for tracking migration and dispersal.

BACKGROUND: Isotopes can provide unique solutions to fundamental problems related to the ecology and evolution of migration and dispersal because prior movements of individuals can theoretically be tracked from tissues collected from a single capture. However, there is still remarkably little information available about how and why isotopes vary in wild animal tissues, especially over large spatial scales. METHODOLOGY/PRINCIPAL FINDINGS: Here, we describe variation in both stable-hydrogen (deltaD(F)) and strontium ((87)Sr/(86)Sr(F)) isotopic compositions in the feathers of a migratory songbird, the Tree Swallow (Tachycineta bicolor), across 18 sampling sites in North America and then examine potential mechanisms driving this variation. We found that deltaD(F) was correlated with latitude of the sampling site, whereas (87)Sr/(86)Sr(F) was correlated with longitude. deltaD(F) was related to deltaD of meteoric waters where molting occurred and (87)Sr/(86)Sr(F) was influenced primarily by the geology in the area where feathers were grown. Using simulation models, we then assessed the utility of combining both markers to estimate the origin of individuals. Using 13 geographic regions, we found that the number of individuals correctly assigned to their site of origin increased from less than 40% using either deltaD or (87)Sr/(86)Sr alone to 74% using both isotopes. CONCLUSIONS/SIGNIFICANCE: Our results suggest that these isotopes have the potential to provide predictable and complementary markers for estimating long-distance animal movements. Combining isotopes influenced by different global-scale processes may allow researchers to link the population dynamics of animals across large geographic ranges.

Continent-wide variation in feather colour of a migratory songbird in relation to body condition and moulting locality.

Understanding the causes of variation in feather colour in free-living migratory birds has been challenging owing to our inability to track individuals during the moulting period when colours are acquired. Using stable-hydrogen isotopes to estimate moulting locality, we show that the carotenoid-based yellow-orange colour of American redstart (Setophaga ruticilla) tail feathers sampled on the wintering grounds in Central America and the Caribbean is related to the location where feathers were grown the previous season across North America. Males that moulted at southerly latitudes were more likely to grow yellowish feathers compared with males that moulted more orange-red feathers further north. Independent samples obtained on both the breeding and the wintering grounds showed that red chroma-an index of carotenoid content-was not related to the mean daily feather growth rate, suggesting that condition during moult did not influence feather colour. Thus, our results support the hypothesis that feather colour is influenced by ecological conditions at the locations where the birds moulted. We suggest that these colour signals may be influenced by geographical variation in diet related to the availability of carotenoids.

Hydrogen isotopic variation in migratory bird tissues of known origin: implications for geographic assignment.

Continent-wide variation in hydrogen isotopic composition of precipitation is incorporated into animal diets, providing an intrinsic marker of geographic location at the time of tissue growth. Feathers from migratory birds are now frequently analyzed for stable-hydrogen isotopes (deltaD) to estimate the location of individuals during a preceding molt. Using known-origin birds, we tested several assumptions associated with this emerging technique. We examined hydrogen isotopic variation as a function of age, sex, feather type and the timing of molt in a marked population of American redstarts (Setophaga ruticilla) breeding in southeastern Ontario. We measured deltaD in feathers and blood from individuals that bred or hatched at our study site during the year in which those tissues were grown. Juvenile tissues from 5- to 10-day-old birds had more negative deltaD values than those from adults, which most likely reflected age-related differences in diet. Within adults, primary feathers had more negative deltaD values than contour feathers. The mean deltaD value in adult primary feathers was relatively consistent among years and with the value expected for our study population. However, among-individual variation in deltaD corresponded to an estimated latitudinal range of 6-8 degrees (650-900 km). We conclude that feathers sampled from recently hatched juveniles may not provide a reliable estimate of expected local isotopic signatures for comparison with adult feathers of unknown origin. Furthermore, we urge researchers to use caution when using deltaD values in feathers to infer geographic origin, and suggest that the best approach is to assign individuals to broad geographic zones within a species' potential molting range.

Reproductive effort, molting latitude, and feather color in a migratory songbird.

Toward the end of the breeding season, migratory songbirds face crucial tradeoffs between the timing of reproduction, molt, and migration. Using stable hydrogen isotopes, we show that male American redstarts investing in high levels of reproduction late in the season adopt a unique strategy of combining molt and migration. Tail feathers molted during migration also reflect less orange-red light, indicating reduced carotenoid concentration. Thus, we show how reproduction in a migratory animal can influence both life history strategies (location of molt) and social signals (feather color) during subsequent periods of the annual cycle.