Determining origin in a migratory marine vertebrate: a novel method to integrate stable isotopes and satellite tracking

Stable isotope analysis is a useful tool to track animal movements in both terrestrial and marine environments. These intrinsic markers are assimilated through the diet and may exhibit spatial gradients as a result of biogeochemical processes at the base of the food web. In the marine environment, maps to predict the spatial distribution of stable isotopes are limited, and thus determining geographic origin has been reliant upon integrating satellite telemetry and stable isotope data. Migratory sea turtles regularly move between foraging and reproductive areas. Whereas most nesting populations can be easily accessed and regularly monitored, little is known about the demographic trends in foraging populations. The purpose of the present study was to examine migration patterns of loggerhead nesting aggregations in the Gulf of Mexico (GoM), where sea turtles have been historically understudied. Two methods of geographic assignment using stable isotope values in known-origin samples from satellite telemetry were compared: (1) a nominal approach through discriminant analysis and (2) a novel continuous-surface approach using bivariate carbon and nitrogen isoscapes (isotopic landscapes) developed for this study. Tissue samples for stable isotope analysis were obtained from 60 satellite-tracked individuals at five nesting beaches within the GoM. Both methodological approaches for assignment resulted in high accuracy of foraging area determination, though each has advantages and disadvantages. The nominal approach is more appropriate when defined boundaries are necessary, but up to 42% of the individuals could not be considered in this approach. All individuals can be included in the continuous-surface approach, and individual results can be aggregated to identify geographic hotspots of foraging area use, though the accuracy rate was lower than nominal assignment. The methodological validation provides a foundation for future sea turtle studies in the region to inexpensively determine geographic origin for large numbers of untracked individuals. Regular monitoring of sea turtle nesting aggregations with stable isotope sampling can be used to fill critical data gaps regarding habitat use and migration patterns. Probabilistic assignment to origin with isoscapes has not been previously used in the marine environment, but the methods presented here could also be applied to other migratory marine species

Combining Models of Environment, Behavior, and Physiology to Predict Tissue Hydrogen and Oxygen Isotope Variance Among Individual Terrestrial Animals

Variations in stable hydrogen and oxygen isotope ratios in terrestrial animal tissues are used to reconstruct origin and movement. An underlying assumption of these applications is that tissues grown at the same site share a similar isotopic signal, representative of the location of their origin. However, large variations in tissue isotopic compositions often exist even among conspecific individuals within local populations, which complicates origin and migration inferences. Field-data and correlation analyses have provided hints about the underlying mechanisms of within-site among-individual isotopic variance, but a theory explaining the causes and magnitude of such variance has not been established. Here we develop a mechanistic modeling framework that provides explicit predictions of the magnitude, patterns, and drivers of isotopic variation among individuals living in a common but environmentally heterogeneous habitat. The model toolbox includes isoscape models of environmental isotopic variability, an agent-based model of behavior and movement, and a physiology-biochemistry model of isotopic incorporation into tissues. We compare model predictions against observed variation in hatch-year individuals of the songbird Spotted Towhee (Pipilo maculatus) in Red Butte Canyon, Utah, and evaluate the ability of the model to reproduce this variation under different sets of assumptions. Only models that account for environmental isotopic variability predict a similar magnitude of isotopic variation as observed. Within the modeling framework, behavioral rules and properties govern how animals nesting in different locations acquire resources from different habitats, and birds nesting in or near riparian habitat preferentially access isotopically lighter resources than those associated with the meadow and slope habitats, which results in more negative body water and tissue isotope values. Riparian nesters also have faster body water turnover and acquire more water from drinking (vs. from food), which exerts a secondary influence on their isotope ratios. Thus, the model predicts that local among-individual isotopic variance is linked first to isotopic heterogeneity in the local habitat, and second to how animals sample this habitat during foraging. Model predictions provide insight into the fundamental mechanisms of small-scale isotopic variance and can be used to predict the utility of isotope-based methods for specific groups or environments in ecological and forensic research.</jats:p

Energetic basis of colonial living in social insects

Understanding the ecology and evolution of insect societies requires greater knowledge of how sociality affects the performance of whole colonies. Metabolic scaling theory, based largely on the body mass scaling of metabolic rate, has successfully predicted many aspects of the physiology and life history of individual (or unitary) organisms. Here we show, using a diverse set of social insect species, that this same theory predicts the size dependence of basic features of the physiology (i.e., metabolic rate, reproductive allocation) and life history (i.e., survival, growth, and reproduction) of whole colonies. The similarity in the size dependence of these features in unitary organisms and whole colonies points to commonalities in functional organization. Thus, it raises an important question of how such evolutionary convergence could arise through the process of natural selection

Optimizing stable isotope sampling design in terrestrial movement ecology research

The recognition of adequate sampling designs is an interdisciplinary topic that has gained popularity over the last decades. In ecology, many research questions involve sampling across extensive and complex environmental gradients. This is the case for stable isotope analyses, which are widely used to characterize large-scale movement patterns and dietary preferences of organisms across taxa. Because natural-abundance stable isotope variation in the environment is incorporated into inert animal tissues, such as feathers or hair, it is possible to draw inferences about the type of food and water resources that individuals consumed and the locations where tissues were synthesized. However, modern stable isotope research can benefit from the implementation of robust statistical analyses and well-designed sampling approaches to improve geographic assignment interpretation. We employed hydrogen stable isotope simulations to study inferences regarding the probability of origin of migratory individuals and reveal gaps in sampling efforts while highlighting uncertainties of assignment model extrapolations. We present an integrative approach that explores multiple sampling strategies across species with different geographic ranges to understand advantages and limitations of animal movement inferences based on stable isotope data. We show the characteristics of different sampling strategies through geographic and isotopic gradients and establish a set of diagnostic tools that uncover the attributes of these gradients and evaluate uncertainties of model results. Our analysis demonstrates that sampling regimes should be evaluated in relation to specific research questions and study constraints, and that adopting a single method across species ranges can lead to a costly but less effective sampling strategy

Advancing interpretation of stable isotope assignment maps: comparing and summarizing origins of known-provenance migratory bats

Probability-of-origin maps deduced from stable isotope data are important for inferring broad-scale patterns of animal migration, but few resources and tools for interpreting and validating these maps exist. For example, quantitative tools for comparing multiple probability-of-origin maps do not exist, and many existing approaches for geographic assignment of individuals have not been validated or compared with respect to precision and accuracy. To address these challenges, we created and analyzed probability-of-origin maps using stable hydrogen isotope values from known-origin individuals of three species of migratory bat. We used a metric of spatial overlap to group individuals by areas of origin without a priori knowledge of such regions. The metric of spatial similarity allowed for quantitative comparison of geographic origins and grouping of individuals with similar origins. We then compared four approaches for inferring origins (cumulative-sum, odds-ratio, quantile-only, and quantile-simulation) across a range of thresholds and probable minimum distance traveled. The accuracy of geographic origins and minimum distance traveled varied across species at most threshold values for most approaches. The cumulative-sum and quantile-simulation approaches had generally higher precision at a given level of accuracy than the odds-ratio and quantile-only approaches, and many threshold values were associated with a relatively high degree (> 300 km) of variation in minimum distance traveled. Overall, these results reinforce the importance of validating assignment techniques with known-origin individuals when possible. We present the tools discussed as part of an R package, ‘isocat’ (“Isotope Origin Clustering and Assignment Tools”)

Biomarkers Reveal Sea Turtles Remained In Oiled Areas Following The Deepwater Horizon Oil Spill

Assessments of large-scale disasters, such as the Deepwater Horizon oil spill, are problematic because while measurements of post-disturbance conditions are common, measurements of pre-disturbance baselines are only rarely available. Without adequate observations of pre-disaster organismal and environmental conditions, it is impossible to assess the impact of such catastrophes on animal populations and ecological communities. Here, we use long-term biological tissue records to provide pre-disaster data for a vulnerable marine organism. Keratin samples from the carapace of loggerhead sea turtles record the foraging history for up to 18 years, allowing us to evaluate the effect of the oil spill on sea turtle foraging patterns. Samples were collected from 76 satellite-tracked adult loggerheads in 2011 and 2012, approximately one to two years after the spill. Of the 10 individuals that foraged in areas exposed to surface oil, none demonstrated significant changes in foraging patterns post spill. The observed long-term fidelity to foraging sites indicates that loggerheads in the northern Gulf of Mexico likely remained in established foraging sites, regardless of the introduction of oil and chemical dispersants. More research is needed to address potential long-term health consequences to turtles in this region. Mobile marine organisms present challenges for researchers to monitor effects of environmental disasters, both spatially and temporally. We demonstrate that biological tissues can reveal long-term histories of animal behavior and provide critical pre-disaster baselines following an anthropogenic disturbance or natural disaster

Individual specialists in a generalist population: results from a long-term stable isotope series

Individual variation in resource use has often been ignored in ecological studies, but closer examination of individual patterns through time may reveal significant intrapopulation differences. Adult loggerhead sea turtles (Caretta caretta) are generalist carnivores with a wide geographical range, resulting in a broad isotopic niche. We microsampled scute, a persistent and continuously growing tissue, to examine long-term variation in resource use (up to 12 years) in 15 nesting loggerhead turtles. Using stable isotopes of nitrogen and carbon, we examined the resource use patterns (integration of diet, habitat and geographical location) and demonstrate that individual loggerheads are long-term specialists within a generalist population. We present our results in the context of a conceptual model comparing isotopic niches in specialist and generalist populations. Individual consistency may have important ecological, evolutionary and conservation consequences, such as the reduction of intraspecific competition

Expanding the isotopic toolbox: Applications of hydrogen and oxygen stable isotope ratios to food web studies

The measurement of stable carbon (δ13C) and nitrogen (δ15N) isotopes in tissues of organisms has formed the foundation of isotopic food web reconstructions, as these values directly reflect assimilated diet. In contrast, stable hydrogen (δ2H) and oxygen (δ18O) isotope measurements have typically been reserved for studies of migratory origin and paleoclimate reconstruction based on systematic relationships between organismal tissue and local environmental water. Recently, innovative applications using δ2H and, to a lesser extent, δ18O values have demonstrated potential for these elements to provide novel insights in modern food web studies. We explore the advantages and challenges associated with three applications of δ2H and δ18O values in food web studies. First, large δ2H differences between aquatic and terrestrial ecosystem end members can permit the quantification of energy inputs and nutrient fluxes between these two sources, with potential applications for determining allochthonous vs. autochthonous nutrient sources in freshwater systems and relative aquatic habitat utilization by terrestrial organisms. Next, some studies have identified a relationship between δ2H values and trophic position, which suggests that this marker may serve as a trophic indicator, in addition to the more commonly used δ15N values. Finally, coupled measurements of δ2H and δ18O values are increasing as a result of reduced analytical challenges to measure both simultaneously and may provide additional ecological information over single element measurements. In some organisms, the isotopic ratios of these two elements are tightly coupled, whereas the isotopic disequilibrium in other organisms may offer insight into the diet and physiology of individuals. Although a coherent framework for interpreting δ2H and δ18O data in the context of food web studies is emerging, many fundamental uncertainties remain. We highlight directions for targeted research that will increase our understanding of how these markers move through food webs and reflect ecological processes

Data From: Dynamic environments generate geographic fluctuations in population structure of an inland shorebird

&lt;p&gt;Data From: Dynamic environments generate geographic fluctuations in population structure of an inland shorebird. Table S1. Samples IDs, age class (adult = after hatch year; AHY) and young (juvenile = hatch year; HY), δ²H values from feathers, and year of collection at the wintering ground (Imperial County, California, USA).&lt;/p&gt

Alternate migration strategies of eastern monarch butterflies revealed by stable isotopes

Alternative life history strategies are mechanisms by which organisms are able to maximize fitness across a range of environmental conditions. Fitness is maximized by different strategies depending on context, resulting in trade-offs between life history strategies. Monarch butterflies (Danaus plexippus) employ both migratory and resident life history strategies. Since residents breed throughout the year, but migrants overwinter in reproductive diapause, there are fitness trade-offs between the two strategies. We used stable isotope analysis to evaluate the geographic origins of monarchs in a yearround population in south Florida. Based on stable isotope profiles of hydrogen and carbon (δ2H and δ13C values), we found that 48% (16/33) of monarchs collected in south Florida are migrants that originated from outside the sampling region. Migrants had a larger wing length than residents; thus, switching to a resident strategy could alter their probability of reproductive success. Further work is needed to investigate the mechanism underlying this pattern, but these findings show that alternate life history strategies and sex-specific behaviors are underexplored factors influencing monarch migration and evolution