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

The early bird gets the shrimp: confronting assumptions of isotopic equilibrium and homogeneity in a wild bird population

Journal of Animal Ecology, 2012

1. Because stable isotope distributions in organic material vary systematically across energy gradients that exist in ecosystems, community and population structures, and in individual physiological systems, isotope values in animal tissues have helped address a broad range of questions in animal ecology. It follows that every tissue sample provides an isotopic profile that can be used to study dietary or movement histories of individual animals. Interpretations of these profiles depend on the assumption that metabolic pools are isotopically well mixed and in equilibrium with dietary resources prior to tissue synthesis, and they extend to the population level by assuming isotope profiles are identically distributed for animals using the same proximal dietary resource. As these assumptions are never fully met, studying structure in the variance of tissue isotope values from wild populations is informative. 2. We studied variation in d 13 C, d 15 N, d 2 H and d 18 O data for feathers from a population of eared grebes (Podiceps nigricollis) that migrate to Great Salt Lake each fall to moult feathers. During this time, they cannot fly and feed almost exclusively on superabundant brine shrimp (Artemia franciscana). The ecological simplicity of this situation minimized the usual spatial and trophic complexities often present in natural studies of feather isotope values. 3. Ranges and variances of isotope values for the feathers were larger than those from previously published studies that report feather isotopic variance, but they were bimodally distributed in all isotope dimensions. Isotope values for proximal dietary resources and local surface water show that some of the feathers we assumed to have been grown locally must have been grown before birds reached isotopic equilibrium with local diet or immediately prior to arrival at Great Salt Lake. 4. Our study provides novel insights about resource use strategies in eared grebes during migration. More generally, it demonstrates the utility of studying variance structures and questioning assumptions implicit in the interpretation of stable isotope data from wild animals.

Linking Hydrogen (δ2H) Isotopes in Feathers and Precipitation: Sources of Variance and Consequences for Assignment to Isoscapes

BACKGROUND: Tracking small migrant organisms worldwide has been hampered by technological and recovery limitations and sampling bias inherent in exogenous markers. Naturally occurring stable isotopes of H (δ(2)H) in feathers provide an alternative intrinsic marker of animal origin due to the predictable spatial linkage to underlying hydrologically driven flow of H isotopes into foodwebs. This approach can assess the likelihood that a migrant animal originated from a given location(s) within a continent but requires a robust algorithm linking H isotopes in tissues of interest to an appropriate hydrological isotopic spatio-temporal pattern, such as weighted-annual rainfall. However, a number of factors contribute to or alter expected isotopic patterns in animals. We present results of an extensive investigation into taxonomic and environmental factors influencing feather δ(2)H patterns across North America. PRINCIPAL FINDINGS: Stable isotope data were measured from 544 feathers from 40 species and 140 known locations. For δ(2)H, the most parsimonious model explaining 83% of the isotopic variance was found with amount-weighted growing-season precipitation δ(2)H, foraging substrate and migratory strategy. CONCLUSIONS/SIGNIFICANCE: This extensive H isotopic analysis of known-origin feathers of songbirds in North America and elsewhere reconfirmed the strong coupling between tissue δ(2)H and global hydrologic δ(2)H patterns, and accounting for variance associated with foraging substrate and migratory strategy, can be used in conservation and research for the purpose of assigning birds and other species to their approximate origin.

Estimating Ecologically Meaningful Isotopic Differences in Observational Studies of Wild Animals

In ecological studies of wildlife movements and foraging, both biologging and isotopic data are routinely collected and increasingly analyzed in tandem. Such analyzes inherit two shortcomings: (1) small sample size linked with the number of telemetric tags that can be deployed, and (2) the observational nature of isotopic gradients. Wildlife ecologists are thus put in a statistical conundrum known as the small n, large p problem. Methods: Using shrinkage regression, which directly addresses the issue of accurately estimating effects from sparse data, we studied what counts as a biologically meaningful isotopic difference (a prerequisite to delineate isoscapes) in the southern elephant seal (Mirounga leonina), a large and elusive marine predator. Results: Seals foraging in Antarctic waters had a lower carbon isotopic value (by ≈ 2‰) than seals foraging either in the interfrontal zone or on the Kerguelen Plateau. The latter two foraging strategies were indistinguishable on the sole basis of δ 13 C values with our data. Conclusions: Shrinkage regression is a conservative statistical technique that has wide applicability in isotopic ecology to help separating robust biological signals from noise.

Stable hydrogen isotope (δD) values in songbird nestlings: effects of diet, temperature, and body size

Canadian Journal of Zoology, 2009

Stable hydrogen isotopes (dD) can be a powerful tool for estimating the large-scale movements of animals, but the cause and extent of isotopic variation within animal tissues remain poorly understood. Here, we simultaneously examined three hypotheses to explain dD variation in the blood (dDB) of nestling Tree Swallows (Tachycineta bicolor (Vieillot, 1808)) from a single nest-box population in southern Ontario, Canada: (1) microgeographic and (or) temporal variation in dD of local diet, (2) potential evaporation of protium resulting from variation in nest-box temperature, and (3) differences in body size resulting in higher rates of water loss and isotope fractionation in larger birds. dDB ranged from -128% to -94%, with a mean ± SD of -113% ± 7%. Nest-box temperatures ranged from 21.5 to 38 8C immediately prior to blood collection. A general linear mixed-effects model explained 80% of the variation in dDB and provided evidence that dD values in prey, maximum temperature 1 day prior to blood collection, and body size were all significant predictors of dDB. Our results suggest that isotopic variation in individuals and local populations arises from a combination of physiological factors and local environmental variation. To gain a complete understanding of how dD values can be used to estimate animal movements, additional work is needed to determine how these factors influence other tissues, such as metabolically inert feathers, and animals of different age classes.

Assigning birds to geographic origin using feather hydrogen isotope ratios (δ 2 H): importance of year, age, and habitat

Canadian Journal of Zoology, 2012

In North America, gradients in the ratio of stable hydrogen isotopes in amount-weighted, growing-season mean precipitation (2H:1H; depicted as δ2Hp) form a largely latitude-sensitive isoscape that can be used to estimate the geographical origin of animals. Feathers are metabolically inert following growth and δ2Hf values retain information on geographical origins. However, there are important assumptions underlying this approach that can only be tested using birds of known origin. Here, we investigated sources of variation in δ2Hf measurements from Ovenbirds ( Seiurus aurocapilla (L., 1766)) associated with year, age class, feather type, season, and habitat type in New Brunswick, Canada. The observed δ2Hf generally followed that predicted from the Global Network of Isotopes in Precipitation database. However, we found a strong year × age interaction on δ2Hf. Season, habitat type, and feather type explained only a small portion of the overall variation in δ2Hf. These results show the...

How large is large: estimating ecologically meaningful isotopic differences in observational studies of wild animals

RATIONALE: In ecological studies of wildlife movements and foraging, bio-logging and isotopic data are routinely collected and increasingly analyzed in tandem. Such analyses have two shortcomings: (1) small sample size linked with the number of telemetric tags that can be deployed, and (2) the observational nature of isotopic gradients. Wildlife ecologists are thus put in a statistical conundrum known as the small n, large p problem. METHODS: Using shrinkage regression, which directly addresses the issue of accurately estimating effects from sparse data, we studied what counts as a biologically meaningful isotopic difference (a prerequisite to delineate isoscapes) in the southern elephant seal (Mirounga leonina), a large and elusive marine predator. RESULTS: Seals foraging in Antarctic waters had a lower carbon isotopic value (by % 2%) than seals foraging either in the interfrontal zone or on the Kerguelen Plateau. The latter two foraging strategies were indistinguishable on the sole basis of d 13 C values with our data. CONCLUSIONS: Shrinkage regression is a conservative statistical technique that has wide applicability in isotopic ecology to help separate robust biological signals from noise.

Tracing Water Sources of Terrestrial Animal Populations with Stable Isotopes: Laboratory Tests with Crickets and Spiders

Fluxes of carbon, nitrogen, and water between ecosystem components and organisms have great impacts across levels of biological organization. Although much progress has been made in tracing carbon and nitrogen, difficulty remains in tracing water sources from the ecosystem to animals and among animals (the ‘‘water web’’). Naturally occurring, nonradioactive isotopes of hydrogen and oxygen in water provide a potential method for tracing water sources. However, using this approach for terrestrial animals is complicated by a change in water isotopes within the body due to differences in activity of heavy and light isotopes during cuticular and transpiratory water losses. Here we present a technique to use stable water isotopes to estimate the mean mix of water sources in a population by sampling a group of sympatric animals over time. Strong correlations between H and O isotopes in the body water of animals collected over time provide linear patterns of enrichment that can be used to predict a mean mix of water sources useful in standard mixing models to determine relative source contribution. Multiple temperature and humidity treatment levels do not greatly alter these relationships, thus having little effect on our ability to estimate this population-level mix of water sources. We show evidence for the validity of using multiple samples of animal body water, collected across time, to estimate the isotopic mix of water sources in a population and more accurately trace water sources. The ability to use isotopes to document patterns of animal water use should be a great asset to biologists globally, especially those studying drylands, droughts, streamside areas, irrigated landscapes, and the effects of climate change.

An Isotopic Exploration of the Potential of Avian Tissues to Track Changes in Terrestrial and Marine Ecosystems

2007

Birds are among the most successful of all vertebrates and currently occupy all of the earth's major ecosystems. Birds have evolved to exploit an impressive array of niches within habitats of both terrestrial and marine biomes where they range from extreme dietary specialists to generalists. This broad trophic diversity includes frugivory and nectarivory to piscivory and carnivory. Birds are also among the most volant of all life forms and several species migrate annually between breeding and wintering sites that may be many thousands of kilometers apart. Birds are also conspicuous, accessible, and amenable to scientific investigation, and there is a good deal of interest in using birds as indicators of ecological change at various spatial and temporal scales. They also produce a range of tissues that are amenable to dietary reconstruction using stable isotopes and so there is a growing interest in using isotopic measurements of birds to monitor larger-scale ecological processes that are associated with characteristic isotopic abundance. This chapter reviews how the isotopic measurement of avian tissues can be used to monitor ecological change. Here, ecological change is considered to be both changes in baseline food web isotopic composition and ecological changes involving the birds themselves (i.e., using stable isotopes to investigate how birds respond to environmental change).

Using Isotopic Variance to Detect Long-Distance Dispersal and Philopatry in Birds: An Example with Ovenbirds and American Redstarts

The Condor, 2004

Understanding movements of individual birds between breeding sites (breeding dispersal) or between natal sites and the site of first breeding (natal dispersal) is crucial to the modeling of population dynamics. Unfortunately, these aspects of demography are poorly understood for avian species in general, and for migratory songbirds in particular. This is because it is often impossible to sample broadly enough to relocate marked birds that have moved. We used stable-hydrogen (␦D) and carbon (␦ 13 C) isotope analyses of the feathers of 139 American Redstarts (Setophaga ruticilla) and 193 Ovenbirds (Seiurus aurocapillus) to evaluate evidence for individuals molting feathers at locations other than their breeding sites from the previous year. We sampled outer rectrices from breeding populations at three extensive boreal forest sites (Prince Albert National Park and Duck Mountain, Saskatchewan, and Lac La Biche, Alberta) and at three isolated forest tracts (Cypress Hills, and Moose Mountain, Saskatchewan, and Turtle Mountain, Manitoba) in western Canada. Based on outlier analysis of ␦D measurements, we found evidence for long-distance dispersal ranging from 0-29% of individuals. For both species, second-year birds had higher variance in ␦D values suggesting they had a higher probability of originating from elsewhere compared to after-second-year birds.