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

Abstract

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.

Compound-Specific Stable Isotope Analysis of Amino Acids in Pelagic Shark Vertebrae Reveals Baseline, Trophic, and Physiological Effects on Bulk Protein Isotope Records

“…Future research should explore how spatio-temporal variation in isotopic baselines, migration and tissue isotopic discrimination interact to influence tissue isotopic compositions in pelagic sharks. Such space-time isotope dynamics can be explored using a simulation modeling framework combining isoscape models, agent-based models of behavior and movement, and physiology-biochemistry models (e.g., Carpenter-Kling et al, 2019;Magozzi et al, 2020). Furthermore, additional controlled-feeding experiments such as those by Wang et al (2019) are required to better constrain trophic and physiological influences on δ 13 C values of nonessential amino acids.…”

Temporal stability of δ2H in insect tissues: Implications for isotope-based geographic assignments

“…Whilst this high intra-site variance does not preclude using δ 2 H geolocation, it sets inherent limits of this geolocation tool to provide specific geographic assignments for migratory insects. Other possible sources of intra-site isotope variance such as variations in the δ 2 H of plants and water at one given site, should be further explored to develop a better understanding and prediction of this uncertainty (e.g., Magozzi et al, 2020). To minimise the uncertainty identified in this study, researchers should be careful to avoid sampling wing portions with veins, and they should also consider sampling individuals of similar ages (using for instance similar wing worn indices).…”

A hydrogen isoscape for tracing the migration of herbivorous lepidopterans across the Afro‐Palearctic range

“…mechanisms for the cycling of water between precipitation and larvae. 29,35,76 It is well known that tropical climates differ fundamentally from temperate climates with stochastic inter-annual (e.g. drought versus wet years) and intra-annual (wet and dry season)…”

“…33 Multiple transfer functions have been developed between the δ 2 H in insect wings of known-origin individuals and δ 2 H isoscape of precipitation. 15,18,27,29,34 These different equations exist because (1) approaches and standards used for δ 2 H analysis have not been consistent between studies, 35,36 (2) different known-origin individual sample sets have been produced for different regions, time periods and species, 10,29,[37][38][39] (3) distinct sampling strategies of known-origin sample sets on a given area can produce different equations 40 and (4) distinct global isoscapes of δ 2 H in precipitation have been used as base maps to compare to known-origin sample sets. 22,41,42 Despite these inconsistencies, the existing δ 2 H transfer functions, which might be specific to a species, time, location and reference material, are often applied indiscriminately to study insect dispersal and migration, yielding ecological interpretations that might not rigorously incorporate uncertainty.…”