Measures of physiological stress: a transparent or opaque window into the status, management and conservation of species? (original) (raw)
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Measuring stress in wildlife: techniques for quantifying glucocorticoids
Oecologia, 2011
Stress responses play a key role in allowing animals to cope with change and challenge in the face of both environmental certainty and uncertainty. Measurement of glucocorticoid levels, key elements in the neuroendocrine stress axis, can give insight into an animal's well-being and can aid understanding ecological and evolutionary processes as well as conservation and management issues. We give an overview of the four main biological samples that have been utilized [blood, saliva, excreta (feces and urine), and integumentary structures (hair and feathers)], their advantages and disadvantages for use with wildlife, and some of the background and pitfalls that users must consider in interpreting their results. The matrix of choice will depend on the nature of the study and of the species, on whether one is examining the impact of acute versus chronic stressors, and on the degree of invasiveness that is possible or desirable. In some cases, more than one matrix can be measured to achieve the same ends. All require a significant degree of expertise, sometimes in obtaining the sample and always in extracting and analyzing the glucocorticoid or its metabolites. Glucocorticoid measurement is proving to be a powerful integrator of environmental stressors and of an animal's condition.
environmental unpredictability shapes glucocorticoid regulation across populations of tree swallows
Nature: Scientific Reports, 2020
The ability to respond appropriately to challenges is an important contributor to fitness. Variation in the regulation of glucocorticoid hormones, which mediate the phenotypic response to challenges, can therefore influence the ability to persist in a given environment. We compared stress responsiveness in four populations of tree swallows (Tachycineta bicolor) breeding under different environmental conditions to evaluate support for different selective pressures in driving the evolution of glucocorticoid regulation. in accordance with the environmental unpredictability hypothesis, stronger stress responses were seen in more unpredictable environments. contrary to the reproductive value hypothesis, the stress response was not lower in populations engaging in more valuable reproductive attempts. populations with stronger stress responses also had stronger negative feedback, which supports a "mitigating" rather than a "magnifying" effect of negative feedback on stress responses. these results suggest that combining a robust stress response with strong negative feedback may be important for persisting in unpredictable or rapidly changing environments. Global environmental changes are altering the habitats of many species 1. For species with wide geographic ranges, intra-specific variation in life-history strategies resulting from historical selection might predispose some populations to be more or less susceptible to increasing environmental changes 2-4. Environmental variation favours individuals that differentially allocate time and energy to reproduction and self-maintenance in order to maximize lifetime fitness 5-7. Thus, characterizing differences in the regulation of this trade-off across environments is critical for understanding the mechanisms that have shaped phenotypic responses and that may allow successful adaptation and population persistence under rapid global changes. While the ultimate reasons for variation in life-history traits across environments and latitudes have been well studied, we have a limited understanding of the proximate mechanisms that underlie this variation 8,9. Because environmental factors may influence the evolution of life-history traits by acting on physiological systems that integrate external conditions, hormones have been proposed to play a crucial role as mediators of life-history trade-offs 5,9,10. The hypothalamic-pituitary-adrenal (HPA) axis is a fundamental component of the endocrine system that forms an interface between an animal and its environment 11-13. The HPA axis coordinates the response to energetic and other challenges mainly by regulating the production and release of glucocorticoids 14,15. In non-stressed individuals, glucocorticoids are usually maintained at low levels to regulate energy balance and mediate foraging and other locomotor activities 14,16. When facing unpredictable challenges, circulating glucocorticoids increase dramatically, promoting a suite of processes that facilitate responding to and recovering from these challenges 14,15. When sustained, this stress response can trigger an emergency life-history stage in which breeding activities are usually reduced, and energy is redirected toward survival 15. Thus, glucocorticoids-particularly in the presence of a stressor-have been widely predicted to mediate life history trade-offs between current and future reproduction. While models of the stress response make clear predictions about redirecting effort, empirical studies have proved equivocal in linking environmental conditions to appropriate responses. One limitation of much empirical work to date is that it has focused on the relationship between glucocorticoids and fitness in a single context (i.e., a single population, year, or environment) 12,17. The factors that shape these relationships are best understood by open
Conservation Physiology, 2020
Plasma glucocorticoid (CORT) levels are one measure of stress in wildlife and give us insight into natural processes relevant to conservation issues. Many studies use total CORT concentrations to draw conclusions about animals'stress state and response to their environment. However, the blood of tetrapods contains corticosteroid-binding globulin (CBG), which strongly binds most circulating CORT. Only free CORT (CORT not bound by CBG) leaves the circulation and exerts biological effects on CORT-sensitive tissues. Measuring free CORT concentrations provides insight to an animal's stress response that cannot be revealed by simply measuring total CORT. To calculate free CORT concentrations in plasma or serum samples, one needs three measurements: the binding affinity of CBG for CORT (which varies by species), the total CORT concentration in the sample and the maximum corticosteroid binding capacity (MCBC) of CBG in the sample. Here, we detail the measurement of CBG binding capacity. We compare and contrast the three main methods to measure MCBC: charcoal, cell harvester and dialysis. Each is defined by the means by which free and bound CORT are separated. We weigh the relative merits and challenges of each. We conclude that sample volume, species and taxon binding specificity, and availability of equipment are the primary considerations in selecting the appropriate separation method. For most mammals, the charcoal method is recommended. For birds, the harvester method has critical advantages over the charcoal method. The dialysis method is widely regarded as the gold standard and has lower equipment costs but is more time-intensive and costly in terms of radioactive isotope needed and is less suited to processing large numbers of samples. The binding capacity of CBG varies tremendously within and among the bird and marine mammal species studied, and we discuss the implication of this variation for understanding the role of stress in wildlife.
2016
Stress responses play a key role in allowing animals to cope with change and challenge in the face of both environmental certainty and uncertainty. Measure-ment of glucocorticoid levels, key elements in the neuro-endocrine stress axis, can give insight into an animal’s well-being and can aid understanding ecological and evo-lutionary processes as well as conservation and manage-ment issues. We give an overview of the four main biological samples that have been utilized [blood, saliva, excreta (feces and urine), and integumentary structures (hair and feathers)], their advantages and disadvantages for use with wildlife, and some of the background and pitfalls that users must consider in interpreting their results. The matrix of choice will depend on the nature of the study and of the species, on whether one is examining the impact of acute versus chronic stressors, and on the degree of inva-siveness that is possible or desirable. In some cases, more than one matrix can be measured to ...
IUCN conservation status does not predict glucocorticoid concentrations in reptiles and birds
Integrative and comparative biology, 2018
Circulating glucocorticoids (GCs) are the most commonly used biomarker of stress in wildlife. However, their utility as a tool for identifying and/or managing at-risk species has varied. Here, we took a very broad approach to conservation physiology, asking whether IUCN (International Union for the Conservation of Nature) listing status (concern versus no obvious concern) and/or location within a geographic range (edge versus non-edge) predicted baseline and post-restraint concentrations of corticosterone among many species of birds and reptiles. Even though such an approach can be viewed as coarse, we asked in this analysis whether corticosterone concentrations might be useful to implicate species at risk. Indeed, our effort, relying on HormoneBase, a repository of data on wildlife steroids, complements several other large-scale efforts in this issue to describe and understand GC variation. Using a phylogenetically informed Bayesian approach, we found little evidence that either IU...
Multiple measures elucidate glucocorticoid responses to environmental variation in predation threat
Oecologia, 2011
Predator-induced changes in the glucocorticoid responses of prey have been proposed to mediate indirect predator effects on prey demography. Ambiguities exist, however, as to whether differences in predation threat in the environment at large affect the mean glucocorticoid response in wild birds and mammals, and whether this is likely to affect reproduction. Most studies to date that have examined glucocorticoid responses to environmental variation in predation threat have evaluated just one of the several potential measures of the glucocorticoid response, and this may be the source of many ambiguities. We evaluated multiple measures of the glucocorticoid response [plasma total CORTicosterone, corticosteroid binding globulin (CBG) and free CORT] in male and female song sparrows (Melospiza melodia) sampled at locations differing in predation threat in the environment at large, where we have previously reported reproductive differences suggestive of indirect predator effects. Total CORT varied markedly with predation threat in males but not females whereas the opposite was true for CBG, and both sexes demonstrated the same moderately significant free CORT response. Considering all three indices, a glucocorticoid response to environmental variation in predation threat was evident in both sexes, whereas there were ambiguities considering each index singly. We conclude that collecting multiple physiological measures and conducting multivariate analyses may provide a preferable means of assessing glucocorticoid responses to environmental variation in predation threat, and so help clarify whether such glucocorticoid changes affect reproduction in wild birds and mammals.
Journal of Zoo and Wildlife Medicine, 2006
Conservation medicine is a discipline in which researchers and conservationists study and respond to the dynamic interplay between animals, humans, and the environment. From a wildlife perspective, animal species are encountering stressors from numerous sources. With the rapidly increasing human population, a corresponding increased demand for food, fuel, and shelter; habitat destruction; and increased competition for natural resources, the health and well-being of wild animal populations is increasingly at risk of disease and endangerment. Scientific data are needed to measure the impact that human encroachment is having on wildlife. Nonbiased biometric data provide a means to measure the amount of stress being imposed on animals from humans, the environment, and other animals. The stress response in animals functions via glucocorticoid metabolism and is regulated by the hypothalamic-pituitary-adrenal axis. Fecal glucocorticoids, in particular, may be an extremely useful biometric test, since sample collection is noninvasive to subjects and, therefore, does not introduce other variables that may alter assay results. For this reason, many researchers and conservationists have begun to use fecal glucocorticoids as a means to measure stress in various animal species. This review article summarizes the literature on many studies in which fecal glucocorticoids and their metabolites have been used to assess stress levels in various mammalian species. Variations between studies are the main focus of this review. Collection methods, storage conditions, shipping procedures, and laboratory techniques utilized by different researchers are discussed.
Journal of experimental zoology. Part A, Ecological genetics and physiology, 2013
Habitat can constrain and shape successful ecological and physiological strategies, thus providing the context for the evolution of life-history traits. However, unpredictable challenges, such as storms, natural disasters, and human activities can also have great effects on stress. Glucocorticoids (GCs) are adrenal steroid hormones that play an important role in how vertebrates cope with these predictable and unpredictable environmental challenges. Although assessing GCs levels can have many applications in the study of wildlife and/or captive animals, with or without capturing individuals, it requires a species-specific complete validation (analytical and biological) before its use. In this work, our aim was to: (a) validate a radioimmunoassay (RIA) for measuring GCs levels in L. guanicoe serum; (b) assess cortisol and corticosterone levels (if present) in serum of wild L. guanicoe individuals; and (c) compare the response to acute stressors (handling, shearing, and release). Our results successfully: (a) validated RIA for asses GCs levels in wild ungulates; (b) confirmed the presence for cortisol and corticosterone and showed that both GCs are differently affected by environmental stimuli in L. guanicoe; and (c) showed that GCs exhibit different patterns in the field and in response to acute stressors, making these camelids an interesting endocrinological model when seeking the adaptive functions of a given variation and further emphasizing the complexity of GC physiology in wild mammals.
Hormones and behavior, 2014
A fundamental element of how vertebrates respond to stressors is by rapidly elevating circulating glucocorticoid hormones. Individual variation in the magnitude of the glucocorticoid stress response has been linked with reproductive success and survival. But while the adaptive value of this response is believed to stem in part from changes in the expression of hormone-mediated behaviors, it is not clear how the behavior of stronger and weaker glucocorticoid responders differs during reproduction, or during exposure to ecologically relevant stressors. Here we report that in a population of barn swallows (Hirundo rustica erythrogaster) experiencing high rates of nest predation, circulating levels of corticosterone (the primary avian glucocorticoid) during exposure to a standardized stressor predict aspects of subsequent behavior and fitness. Individuals that mounted a stronger corticosterone stress response during the early reproductive period did not differ in clutch size, but fledge...
Integrative and comparative biology, 2018
Animals go through different life history stages such as reproduction, moult, or migration, of which some are more energy-demanding than others. Baseline concentrations of glucocorticoid hormones increase during moderate, predictable challenges and thus are expected to be higher when seasonal energy demands increase, such as during reproduction. By contrast, stress-induced glucocorticoids prioritize a survival mode that includes reproductive inhibition. Thus, many species down-regulate stress-induced glucocorticoid concentrations during the breeding season. Interspecific variation in glucocorticoid levels during reproduction has been successfully mapped onto reproductive investment, with species investing strongly in current reproduction (fast pace of life) showing higher baseline and lower stress-induced glucocorticoid concentrations than species that prioritize future reproduction over current attempts (slow pace of life). Here we test the "glucocorticoid seasonal plasticity ...