Ontogenetic and sexual characterization of the feeding habits of franciscanas,Pontoporia blainvillei,based on tooth dentin carbon and nitrogen stable isotopes

We assessed the feeding habits of franciscanas (Pontoporia blainvillei) from southern Brazil through carbon and nitrogen stable isotopes measured in the tooth dentin of dolphins from different age classes. Generalized additive models were fitted to assess whether sex, age, and total body length explained changes in franciscanas isotope ratios. Bayesian isotope mixing models were applied to estimate the contributions of prey items, selected based on stomach content analysis (SCA), to franciscanas' diet. Different trophic enrichment factors (TEF) were applied and the results were compared using Bhattachayya's coefficient index to test for differences in model outputs and to define the best TEF for franciscanas. We found different relative importance of the main prey between the methods, and the contribution by squids could be lower than suggested by SCA. Because the dentin deposited during nursing seems to influence the isotopic ratios of juveniles, caution is recommended when interpreting dietary estimates based on whole tooth samples. This study is the first to characterize ontogenetic shifts in franciscanas' feeding habits using stable isotope analysis (SIA) and testing different TEF values. SIA and SCA complement each other in dietary studies, mitigating potential biases resulting from the use of each method separately.     

Development and multiplex PCR amplification of novel microsatellite markers in the White‐tailed Sea Eagle,Haliaeetus albicilla (Aves: Falconiformes,Accipitridae)

We report the development of 14 novel polymorphic microsatellite markers cloned from the White‐tailed Sea Eagle, Haliaeetus albicilla, a formerly threatened raptor that has received much conservation attention throughout Eurasia. We also present a protocol for multiplex polymerase chain reaction (PCR) amplification of the loci. Among 40 unrelated H. albicilla individuals from southern Sweden, the markers produced two to eight alleles per locus, and average observed and expected heterozygosities were 0.463 and 0.468, respectively. We further present five microsatellite markers that appeared monomorphic in H. albicilla, but which may be of interest for use in other raptor species.     

Spatial and temporal variability in ringed seal (Pusa hispida) stable isotopes in the Beaufort Sea

Arctic ecosystem dynamics are shifting in response to warming temperatures and sea ice loss. Such ecosystems may be monitored by examining the diet of upper trophic level species, which varies with prey availability. To assess interannual variation in the Beaufort Sea ecosystem, we examined spatial and temporal trends in ringed seal (Pusa hispida) δ¹³C and δ¹⁵N in claw growth layers grown from 1964 to 2011. Stable isotopes were correlated with climate indices, environmental conditions, seal population productivity, and geographic location. Sex and age did not influence stable isotopes. Enriched ¹³C was linked to cyclonic circulation regimes, seal productivity, and westward sampling locations. Higher δ¹⁵N was linked to lower sea surface temperatures, a higher percentage of pups in the subsistence harvest, and sample locations that were eastward and further from shore. From the 1960s to 2000s, ringed seal niche width expanded, suggesting a diversification of diet due to expansion of prey and/or seal space use. Overall, trends in ringed seal stable isotopes indicate changes within the Beaufort Sea ecosystem affected by water temperatures and circulation regimes. We suggest that continued monitoring of upper trophic level species will yield insights into changing ecosystem structure with climate change.     

Spatial,temporal, age,and sex related variation in the diet of South American sea lions in southern Chile

We analyzed spatial, temporal, and age/sex variation in the diet of the South American sea lions (SASL, Otaria byronia) in southern Chile via δ¹³C and δ¹⁵N isotope analysis, with emphasis on exotic farmed and feral salmonids as a source of prey for this generalist predator. Isotope mixing models show that the primary prey consumed by SASL were demersal and benthopelagic fishes. Individuals sampled in summer and in the outer coast had higher δ¹⁵N values than those from winter or from the inner coast due to consumption of high trophic level demersal fish. We also found evidence of an ontogenetic shift in isotopic niche width as measured by δ¹³C and δ¹⁵N standard ellipse areas, with juveniles showing a restricted isotopic niche width (1.0‰²) in comparison to subadult (2.2‰²) and adult males (1.9‰²). The proportion of salmonids in the diet of the SASL was negligible and lower than reported in previous studies, which may be related to a recent drop in the production of salmon aquaculture in the region. Our study suggests that the SASL are able to adapt to shifts in spatiotemporal variations in the abundance of potential prey, including feral and farmed salmonids.     

Between‐lake variation in the trophic ecology of an invasive crayfish

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The influence of climate and habitat on stable isotope signatures and the isotopic niche of nestling White‐headed Woodpeckers (Dryobates albolarvatus)

The majority of landbird species feed their nestlings arthropods and variation in arthropod populations can impact reproductive outcomes in these species. Arthropod populations in turn are influenced by climate because temperature affects survival and reproduction, and larval development. Thus, climate factors have the potential to influence many bird species during their reproductive phases. In this study, we assessed climate factors that impact the diet of nestling White‐headed Woodpecker (Dryobates albolarvatus), an at‐risk keystone species in much of its range in western North America. To do this, we measured stable isotope signatures (δ¹³C and δ¹⁵N) in 152 nestlings across six years and linked variation in isotopic values to winter (December–February) and spring (June) precipitation and temperature using mixed effects models. We also explored habitat factors that may impact δ¹³C and δ¹⁵N and the relationship between δ¹⁵N and nest productivity. Last, we estimated isotopic niche width for nestlings in different watersheds and years using Bayesian standard ellipses, which allowed us to compare dietary niche width and overlap. We found that colder winter temperatures were associated with an increase in δ¹⁵N and δ¹⁵N levels had a weak positive relationship with nest productivity. We also found that sites with a more diverse tree community were associated with a broader isotopic niche width in nestlings. Our findings suggest that nestling diet is affected by climate, and under future warming climate scenarios, White‐headed Woodpecker nestling diet may shift in favor of lower trophic level prey (prey with lower δ¹⁵N levels). The impact of such changes on woodpecker populations merits further study.     

Temporal variability in stable isotope ratios of C and N in the vibrissa of captive and wild adult South American sea lions Otaria byronia: More than just diet shifts

We analyzed the δ¹³C and δ¹⁵N values in the vibrissae of captive adult breeding South American sea lions (Otaria byronia) fed at a constant diet and then used this information to analyze the change in stable isotope values along the vibrissae from wild individuals. The overall diet‐to‐vibrissa discrimination factor of the captive animals was 3.0‰ ± 0.1‰ for δ¹³C and 3.6‰ ± 0.1‰ for δ¹⁵N, but the stable isotope ratios fluctuated periodically despite constant diet. The δ¹³C and δ¹⁵N values of the captive male declined at the end of the breeding season, whereas the δ¹³C values of the female increased during the central part of pregnancy and the δ¹⁵N values peaked during lactation. The δ¹³C and δ¹⁵N values of adult wild specimens also fluctuated periodically and vibrissae growth rate (0.15 mm/d in both sexes) was slightly lower than in captivity (0.17 mm/d), assuming an annual periodicity for oscillations. Similarities in the amplitude of the cycles of captive and wild males suggested that fasting was probably the main source of periodic variability in the δ¹⁵N of wild males, whereas pregnancy and lactation were probably the main source of periodic variability for the δ¹³C of wild females.     

Combining stable isotope analysis and conventional techniques to improve knowledge of the diet of the European Roller Coracias garrulus

Diet studies are crucial for understanding the ecology and evolution of species, as well as for establishing appropriate conservation and management strategies. However, they remain methodologically challenging due to variation between seasons, sites, sexes or age groups and even variation between individuals. Due to method‐specific characteristics and biases, a combination of existing techniques can overcome the inherent limitations of each technique and provide a more accurate and broad picture of species’ food preferences. Here, we examine diet information obtained using three different assessment methods to better understand the trophic ecology of the European Roller Coracias garrulus, a species targeted by conservation measures in Europe. First, we analysed regurgitated pellets and video‐recordings to report the diet composition of adult and nestling Rollers, respectively. Secondly, we used stable isotope analysis (SIA) to investigate adult sexual diet segregation as well as to confirm the main findings regarding adult and nestling diets obtained through conventional methods. Based on the analysis of pellets, the diet of adult Rollers was dominated by Coleoptera, whereas camera images revealed that the diet of nestlings was dominated by Orthoptera, mainly grasshoppers and bush crickets. Blood isotopic signatures of adult and nestling Rollers confirmed the results obtained through pellet and video‐recording techniques. Of the three methods, pellet analysis provided the most comprehensive trophic information regarding the detectable prey spectrum and prey species contribution, as well as basic diet information for the SIA. Our results also highlight the potential of SIA for assessing intraspecific variation in diet by sampling individuals of known age and sex, which is often unfeasible through conventional approaches. SIA analysis showed no differences in δ¹³C and δ¹⁵N ratios of blood between males and females and a high degree of overlap amongst isotopic niches, suggesting no sex‐specific partitioning in resource use. Overall, we showed that the combination of different methods could be used to gain new and clearer insights into avian trophic ecology that are essential for informing habitat management aiming to improve availability of foraging resources.     

Diet of harbor porpoises along the Dutch coast: A combined stable isotope and stomach contents approach

High stranding frequency of porpoises, Phocoena phocoena, along the Dutch coast since 2006 has led to increased interest in the ecology of porpoises in the North Sea. Stranded porpoises were collected along the Dutch coast (2006–2008) and their diet was assessed through stomach content and stable isotope analysis (δ¹³C and δ¹⁵N) of porpoise muscle and prey. Stable isotope analysis (SIAR) was used to estimate the contribution of prey species to the porpoises' diet. This was compared to prey composition from stomach contents, to analyze differences between long‐ and short‐term diet. According to stomach contents, 90.5% of the diet consisted of gobies, whiting, lesser sandeel, herring, cod, and sprat. Stable isotope analysis revealed that 70‐83% of the diet consisted of poor cod, mackerel, greater sandeel, lesser sandeel, sprat, and gobies, highlighting a higher importance of pelagic, schooling species in the porpoises' diet compared to stomach contents. This could be due to prey distribution as well as differences in behavior of porpoises and prey between the coastal zone and offshore waters. This study supports the need for multi‐method approaches. Future ecological and fishery impact assessment studies and management decisions for porpoise conservation should acknowledge this difference between the long‐ and short‐term diet.     

Resource diversity promotes among‐individual diet variation,but not genomic diversity,in lake stickleback

Many generalist species consist of specialised individuals that use different resources. This within‐population niche variation can stabilise population and community dynamics. Consequently, ecologists wish to identify environmental settings that promote such variation. Theory predicts that environments with greater resource diversity favour ecological diversity among consumers (via disruptive selection or plasticity). Alternatively, niche variation might be a side‐effect of neutral genomic diversity in larger populations. We tested these alternatives in a metapopulation of threespine stickleback. Stickleback consume benthic and limnetic invertebrates, focusing on the former in small lakes, the latter in large lakes. Intermediate‐sized lakes support generalist stickleback populations using an even mixture of the two prey types, and exhibit greater among‐individual variation in diet and morphology. In contrast, genomic diversity increases with lake size. Thus, phenotypic diversity and neutral genetic polymorphism are decoupled: trophic diversity being greatest in intermediate‐sized lakes with high resource diversity, whereas neutral genetic diversity is greatest in the largest lakes.     

Trophic niche partitioning and diet composition of sympatric fin (Balaenoptera physalus) and humpback whales (Megaptera novaeangliae) in the Gulf of Alaska revealed through stable isotope analysis

Fin and humpback whales are large consumers that are often sympatric, effectively sharing or partitioning their use of habitat and prey resources. Stable carbon and nitrogen isotopes in the skin of fin and humpback whales from two regions in the western Gulf of Alaska, Kodiak, and Shumagin Islands, were analyzed to test the hypothesis that these sympatric baleen whales exhibit trophic niche partitioning within these regions. Standard ellipse areas, estimated using Bayesian inference, suggested that niche partitioning between species is occurring in the Kodiak region but not in the Shumagin Islands. Isotopic mixing models based on stable isotopes from whales and local prey samples, were used to estimate possible diet solutions for whales in the Kodiak region. Comparison of isotopic niches and diet models support niche partitioning, with fin whales foraging primarily on zooplankton and humpback whales foraging on zooplankton and small forage fish. The results of this study show that niche partitioning between sympatric species can vary by region and may be the result of prey availability, prey preferences, or both.     

Seasonal and individual predictors of diet in a free‐ranging population of mandrills

Deciphering the dietary habits of a species is central to understanding its ecology, resource requirements, and the evolution of its life history traits. Detailed information on how primates use their environment to address their nutritional needs is available for many primate species. Such basic, but necessary data are, however, fragmented for secretive primates, especially regarding direct behavioral observations of individuals. In this study, we evaluated the impact of seasonality and demographic characteristics on diet and feeding habits in the only free‐ranging population of habituated mandrills (Mandrillus sphinx), a forest‐dwelling species inhabiting the dense humid forests of Central Africa. We collected fine‐grained quantitative data on feeding behavior of 57 individually‐recognized animals of both sexes and different age classes during a 17‐month period. We identified most consumed plant species and determined their abundance in the habitat of the studied mandrills. We showed that diet in this species was extremely diverse and included approximately 150 different plant species, but also mushrooms, invertebrates, and vertebrates. This omnivorous and highly diverse diet presented, however, a clear frugivorous tendency. While we identified three food items largely consumed throughout the year, we also found a strong seasonal signature on diet that was partly, but not only, related to food availability. Age and sex also influenced feeding habits with some feeding specializations according to the individual categories considered and their associated nutritional needs. Our quantitative data provide a basis for future studies examining the nutritional and mineral content of food items, which will further elucidate important aspects of the ecology of this little studied forest primate.     

The diets of humpback whales (Megaptera novaeangliae) on the shelf and oceanic feeding grounds in the western North Pacific inferred from stable isotope analysis

Humpback whales feed on a variety of prey, but significant differences likely occur between regional feeding grounds. In this study, the diets of humpback whales were analyzed by comparing stable isotope ratios in animal tissues at three humpback whale feeding grounds in the Russian Far East: Karaginsky Gulf, Anadyr Gulf, and the Commander Islands. Anadyr Gulf is a neritic zone far from a shelf break, Karaginsky Gulf is a neritic zone close to a shelf break, and the Commander Islands represent an open oceanic ecosystem where whales feed off the shelf break. Samples from the Commander Islands had the lowest mean δ¹³C and δ¹⁵N values (mean ± SE: δ¹³C = ?18.7 ± 0.1, δ¹⁵N = 10.4 ± 0.1) compared to the samples from Karaginsky Gulf (δ¹³C = ?17.2 ± 0.1, δ¹⁵N = 12.7 ± 0.2) and Anadyr Gulf (δ¹³C= ?17.8 ± 0.1, δ¹⁵N = 14.0 ± 0.4). The samples from Anadyr Gulf had the highest δ¹⁵N values, while the samples from Karaginsky Gulf had the highest δ¹³C values. Both δ¹³C and δ¹⁵N values differed significantly among all three areas. Our data support the hypothesis that humpback whales tend to feed on fish in neritic areas and on plankton in deep oceanic waters.     

Age‐related variation in the trophic characteristics of a marsupial carnivore,the Tasmanian devil Sarcophilus harrisii

Age‐related changes in diet have implications for competitive interactions and for predator–prey dynamics, affecting individuals and groups at different life stages. To quantify patterns of variation and ontogenetic change in the diets of Tasmanian devils Sarcophilus harrisii, a threatened marsupial carnivore, we analyzed variation in the stable isotope composition of whisker tissue samples taken from 91 individual devils from Wilmot, Tasmania from December 2014 to February 2017. Both δ¹³C and δ¹⁵N decreased with increasing age in weaned Tasmanian devils, indicating that as they age devils rely less on small mammals and birds, and more on large herbivores. Devils <12 months old had broader group isotopic niches, as estimated by Bayesian standard ellipses (SEA_B mode = 1.042) than devils from 12 to 23 months old (mode = 0.541) and devils ≥24 months old (mode = 0.532). Devils <24 months old had broader individual isotopic niches (SEA_B mode range 0.492–1.083) than devils ≥24 months old (mode range 0.092–0.240). A decrease in δ¹⁵N from the older whisker sections to the more recently grown sections in devils <24 months old likely reflects the period of weaning in this species, as this pattern was not observed in devils ≥24 months old. Our data reveal changes in the isotopic composition of devil whiskers with increasing age, accompanied by a reduction in isotopic variation both among population age classes and within individuals, reflecting the effect of weaning in early life, and a likely shift from an initially diverse diet of small mammals, birds, and invertebrates towards increasing consumption of larger herbivores in adulthood.     

Fine‐scale variation in natural nitrogen isotope ratios of ants

Stable isotopes provide a powerful means of elucidating the trophic ecology of organisms. Analyses of variation in the ratio of nitrogen isotopes (δ¹⁵N) can provide insights into the trophic position of species with broad diets and the ability to occupy multiple positions in food webs, such as ants. The most powerful studies compare subjects across various spatial scales, but to do so, local variation in δ¹⁵N baselines must be taken into account. To date, a wide variety of baseline calibration methods have been employed, leading some authors to suggest that a standard approach is needed, and that the reality of environmental variation necessitates that this should be at fine scales. In this study, we examine the fine‐scale variation in δ¹⁵N value of colonies of the ant Formica kozlovi Dlussky (Hymenoptera: Formicidae: Formicini) along a sloped transect in Mongolia, and compare these with values for associated soils in an effort to shed further light on this issue. We find variation in ant δ¹⁵N to the order of one trophic level (ca. 3‰), over a distance of only 1 km. Ant δ¹⁵N was highly correlated with soil δ¹⁵N, and variation in mineral soil δ¹⁵N explained ca. 81% of the variation in ant δ¹⁵N. This study underlines the importance of local‐scale baseline corrections for isotopic studies, particularly in environments where baseline variation might be expected. It further suggests that δ¹⁵N of mineral soils may provide a suitable baseline for ecological studies of terrestrial arthropods.     

Spatiotemporal and demographic variation in the diet of New Zealand lesser short‐tailed bats (Mystacina tuberculata)

Variation in the diet of generalist insectivores can be affected by site‐specific traits including weather, habitat, and season, as well as demographic traits such as reproductive status and age. We used molecular methods to compare diets of three distinct New Zealand populations of lesser short‐tailed bats, Mystacina tuberculata. Summer diets were compared between a southern cold‐temperate (Eglinton) and a northern population (Puroera). Winter diets were compared between Pureora and a subtropical offshore island population (Hauturu). This also permitted seasonal diet comparisons within the Pureora population. Lepidoptera and Diptera accounted for >80% of MOTUs identified from fecal matter at each site/season. The proportion of orders represented within prey and the Simpson diversity index, differed between sites and seasons within the Pureora population. For the Pureora population, the value of the Simpson diversity index was higher in summer than winter and was higher in Pureora compared to Eglinton. Summer Eglinton samples revealed that juvenile diets appeared to be more diverse than other demographic groups. Lactating females had the lowest dietary diversity during summer in Pureora. In Hauturu, we found a significant negative relationship between mean ambient temperature and prey richness. Our data suggest that M. tuberculata incorporate a narrower diversity of terrestrial insects than previously reported. This provides novel insights into foraging behavior and ecological interactions within different habitats. Our study is the first from the Southern Hemisphere to use molecular techniques to examine spatiotemporal variation in the diet of a generalist insectivore that inhabits a contiguous range with several habitat types and climates.     

Between‐individual variation drives the seasonal dynamics in the trophic niche of a Neotropical marsupial

The dynamics of population niches result from the variation in resource use within individuals and also from the variation between individuals. The prevalence of one mechanism or the other leads to competing hypotheses about the major mechanisms underlying the empirical observations of the contraction/expansion dynamics of the trophic niche in natural populations. In this study, we investigated how within‐ and between‐individual variation in resource use shapes the food niche dynamics of the woolly mouse opossum, Marmosa paraguayana (Didelphimorphia: Didelphidae), in a remnant of the highly seasonal Cerrado in south‐eastern Brazil. To do so, we analysed the faecal samples of live‐trapped individuals to determine their diets within the wet and dry seasons. In addition to a seasonal shift in the composition of the diet, the population trophic niche was significantly wider during the dry season than the wet season. This expansion resulted from larger between‐individual variation in the dry season that was not related to sex preferences, whereas the individual niche widths did not significantly increase from the wet to the dry seasons. Our findings add to the growing list of animal populations that show individual‐level variation in resource use. Furthermore, these results represent a pattern of individual‐level response to seasonal changes that is different from patterns reported for other organisms. We suggest that a pathway to build more realistic foraging models and produce more accurate predictions on population and community dynamics is to consider between‐individual variation and short‐term niche dynamics.     

Evidence for seasonal variation in δ13C and δ18O profiles of Baculites and implications for growth rate

The life histories of ammonites and the life strategies they employed are difficult to assess without robust modern analogues but placing constraints on ammonite growth rates provides a fundamental first step to understanding this abundant, but poorly understood, fossil group. Here we interpret periodic variations in carbon and oxygen stable isotope profiles from Campanian and Maastrichtian ammonites (Baculites) as seasonally driven and use these records to determine their rate of shell precipitation. Several of these samples are housed in museums and were originally prepared using sealants for display and preservation but testing of these sealants indicated no alteration of the isotopic values of treated carbonate. Diagenetic alteration, as determined by shell microstructure, affected the preservation of isotopic signals, resulting in the loss of seasonal variation in less well‐preserved specimens, and the δ¹³C signal is more robust than δ¹⁸O. The periodicity of isotopic profiles from Baculites shells presented here suggest that these organisms grew at rapid rates (c. 340 mm per year), which may imply an r‐type life strategy in which the animals reach maturity quickly, spawn large quantities of progeny, and die at a young age. Because of the potential mobility of Baculites, reconstructing palaeoenvironmental conditions from these isotopic records is challenging and should be conducted cautiously. Unfortunately, well‐preserved Baculites shells much longer than 350 mm are rarely recovered, which complicates the statistical treatment of potential periodicity in isotopic profiles.