Elsevier

General and Comparative Endocrinology

Volume 191, 15 September 2013, Pages 177-189
General and Comparative Endocrinology

Review
A consensus endocrine profile for chronically stressed wild animals does not exist

https://doi.org/10.1016/j.ygcen.2013.06.014Get rights and content

Highlights

  • Review tries to define an “endocrine profile” of chronically stressed wild animals.

  • High variability in the literature suggests a generalized profile may not exist.

  • Chronic stress diagnosis may require multiple changes of glucocorticoid regulation.

  • Direction of change (increase/decrease) may be less important than a change existing.

Abstract

Given the connection between chronic stress and health, there has been a growing emphasis on identifying chronically stressed wild animals, especially in relation to anthropogenic disturbances. There is considerable confusion, however, in how to identify chronically stressed wild animals, but the most common assumption is that measures of glucocorticoid (GC) function will increase. In an attempt to determine an “endocrine profile” of a chronically stressed wild animal, this review collected papers from the literature that measured baseline GC, stress-induced GC, measures of integrated GC, negative feedback, hypothalamic–pituitary–adrenal axis sensitivity, and/or body weight in chronically stressed animals. The collected studies encompassed laboratory and field studies, numerous diverse species, and multiple techniques for inducing chronic stress. Each paper was ranked according to its relevance to wild animals and scored as to whether the measured response increased, decreased, or stayed the same after exposure to chronic stress. The analyses uncovered so much variation between studies that the literature does not support a generalized endocrine profile in how wild animals respond to chronic stress. The common predictions appear to be based almost entirely on theoretical models rather than empirical data. The three most important variables affecting GC responses were the stressors used to induce chronic stress, the potential for those stressors to induce habituation, and the taxon of the focal species. The best approach for identifying a chronically stressed population appears to be documentation of changes at multiple levels of GC regulation, but the direction of the change (increase or decrease) may be relatively unimportant compared to the fact that the response changes at all. The conclusion is that a consistent, predictable, endocrine response to chronic stress, regardless of the protocol used to induce chronic stress and the species under study, does not exist.

Introduction

As suitable habitat continues to decrease due to human-induced habitat destruction and fragmentation, overexploitation of resources and biological invasion (Ayyad, 2003), wild animal populations are increasingly exposed to anthropogenic stressors that the stress response system has not adapted to handle. For the comparative endocrinologist, the consequences of the adaptive stress response system pushed beyond its adaptive capacity in the face of anthropogenic stressors can be an interesting way to study the consequences of a dysregulated endocrine pathway. And the consequences are apparent – studies have shown that human encroachment has a large impact on risk of disease and overall endangerment of wild populations, (Keay et al., 2006) as well as increased pathogen prevalence due to density increases and proximity of farm animals (Aguirre, 2009). Human recreation (Arlettaz et al., 2007, Peden and Schuster, 2008), tourism (Bejder et al., 2006) and construction-related environmental consequences (Currey et al., 2009) can also influence reproduction rates and population numbers. In addition, such human expansion and habitat destruction also results in a growing need for human-mediated conservation efforts, although these tactics, such as translocation, can themselves increase stress exposure (Dickens et al., 2010).

The missing component linking the comparative endocrinologist studying physiological dysregulation and the conservation biologist studying the consequences of anthropogenic stress is the appropriate physiological marker to indicate “chronic stress” in individuals in a population. A number of researchers have proposed that physiological stress responses of affected individuals could provide such a measurement (Cockrem, 2005, Tarlow and Blumstein, 2007, Wikelski and Cooke, 2006). Traditionally, researchers have attempted to diagnose chronic stress by measuring glucocorticoid hormones (Creel et al., 2002, Wasser et al., 1997). However, much of the work is correlative (i.e. chronic stress was not experimentally applied) and the direction of glucocorticoid change is not always consistent. As a result, there is an apparent need for an exact definition of the term “chronic stress” and the physiological parameters that are then reflected by this physiological state. While other researchers in the past, ourselves included, have written about the difficulty defining “chronic stress”, opting instead to describe a theoretical state of physiological dysregulation described as allostatic overload (McEwen and Wingfield, 2003) or homeostatic overload (Romero et al., 2009), in this review, we aim to determine and describe the physiological features of the stress response in a wild vertebrate affected by “chronic stress” as described by the original researchers.

In the wild, a “stressor” is a natural stimulus, such as a predator or storm, that initiates the acute stress response system (Wingfield et al., 2011). In general, a stimulus becomes a stressor when an animal is faced with uncertainty, lack of information, and/or lack of control (Levine and Ursin, 1991). Importantly, a stressor can be something physically missing as much as it is something physically present, as evident by mounting of a stress response due to lack of expected reward (Romero et al., 1995).

The acute stress response consists of a suite of physiological and behavioral changes that are thought to help an animal survive in the wild (Sapolsky et al., 2000). The role of this response (termed the emergency life-history state, (Wingfield et al., 1998) is to temporarily suspend otherwise normal life-history functions, quickly counteract the impact of the stressor, and allow the animal to return to normal activities. There are two major physiological systems activated in response to stressors (Sapolsky et al., 2000). In addition to the quick Fight-or-Flight response activated by the sympathetic nervous system, perception of the stressor initiates the hypothalamic–pituitary–adrenal (HPA) axis. This hormonal cascade culminates in the secretion of glucocorticoid (GC) hormones. Depending on the species, the predominant GC secreted will be either cortisol or corticosterone (for fish and most mammal species, the predominant GC is cortisol, whereas in rodents, birds, amphibians, and reptiles the predominant GC is corticosterone). An important aspect of HPA axis physiology is that once the stressor diminishes or ceases altogether, GC release is quickly shut-off via negative feedback (Dallman and Bhatnagar, 2001, Romero, 2004, Sapolsky et al., 2000).

In contrast, chronic stress occurs when the stress response system has been pushed beyond its normal capacity by either an altered intensity and/or persistence of stressors (Wingfield and Romero, 2001). In such cases, the emergency life-history state becomes extended, normal activities become chronically disrupted, and physiological systems begin to break down (McEwen and Wingfield, 2003, Romero et al., 2009, Sapolsky et al., 2000). Chronic stress effects occur when the stress response itself begins to cause problems, such that the short-term physiological and/or behavioral changes crucial for alleviating or ameliorating the acute stressor no longer aid in survival (McEwen, 1998). For example, long-term release of GC or dysregulation of the HPA axis can disrupt the reproductive hormone axis and reproductive behavior (Berga, 2008) in addition to causing immune system suppression (Dhabhar and McEwen, 1997). More generally, chronic stress causes a host of negative consequences since it is physiologically taxing on the various homeostatic mechanisms throughout the body (Ursin and Olff, 1993).

Chronic stress, therefore, is the physiological state that indicates that animals are no longer functioning within an adaptive capacity – mediators of the stress response have shifted from protective roles to damaging, pathophysiological effects (McEwen and Wingfield, 2010). When aggregated across many individuals in a population, this state could be a potential biological marker for populations at risk due to anthropogenic stressors. Consequently, what is needed is a way to distinguish between the beneficial aspects and the detrimental long-term physiological effects of stress by differentiating between the acute stress response and chronic stress effects.

Although chronic stress has been the subject of extensive biomedical research for decades, far less is known about the physiological manifestations of chronic stress in wild free-living animals. However, this is precisely the information that is needed if we are to apply the concepts of stress in a conservation context. With this in mind, in this review we evaluate both laboratory and field experiments designed to study the effects of chronic stress and determining their relative appropriateness for wild animals. Our overall goal is twofold: assess the potential for a defined GC profile of a chronically stressed wild animal and then illustrate this consensus profile.

To accomplish this goal, we first had to determine how to compare very different studies, many of which were undertaken for very different purposes than the one we are interested in here. We identified five major experimental design variables that impacted how relevant each study was for determining an endocrine profile for a chronically stressed wild animal. These variables included: (1) whether the study used a wild, captive, or laboratory species; (2) whether habituation to the stressors could impact the ultimate responses; (3) the statistical power (i.e. sample size) of the study; (4) the appropriateness of both the type and intensity of the stressor to a wild animal; and (5) the dependent variable that was measured. We then performed a general literature search for studies that investigated the effects of chronic stress on the HPA system and ranked them according to their relevance to wild animals using the above design variables. We conclude by attempting to identify a consensus GC profile of a chronically stressed wild animal and discuss the implications for diagnosing the presence of chronic stress in wild populations.

Section snippets

Literature search

We performed a literature search using Scopus, Web of Science, and Google Scholar search engines. We cross-referenced search terms including: “chronic stress” and glucocorticoid/corticosterone/cortisol or hypothalamic–pituitary–adrenal/HPA or “negative feedback”. We excluded reviews since we were primarily interested in the design and outcome of specific research studies. We also excluded articles that did not tie glucocorticoid changes to chronic stress or papers that only employed a chronic

Overall response to chronic stress

Fig. 1 summarizes the results of the analysis of the six different response variables. The most robust result is clearly a decrease in body weight. Few studies reported no change and no studies reported an increase. Veterinarians have long used a decrease in body weight as an indication that animals are sick or in distress, so it is encouraging that a decrease in body weight was such a consistent response. However, body weight is, at best, an indirect measure of endocrine function. The

Conclusions

Our analyses indicate that the literature provides little guide in how wild animals will respond endocrinologically to stressors that result in chronic stress. The complexity of the stress response system can lead to highly variable outcomes and even models of chronic stress that have been tested in the laboratory for decades can yield very different results (Patchev and Patchev, 2006). What our analyses make clear is that common predictions on how wild animals will respond to chronic stress

Acknowledgments

We thank L. Butler, R de Bruijn, C. Bauer, and C. Lattin for theoretical discussions. This work was supported by NSF grant IRFP 0910495 and NIH grant F32 HD072732-01 to MJD and NSF grant IOS-1048529 to LMR.

References (59)

  • L. Jacobson

    Hypothalamic–pituitary-adrenocortical axis regulation

    Endocrinol. Metab. Clin. North Am.

    (2005)
  • O. MartÌ et al.

    Anterior pituitary response to stress: time-related changes and adaptation

    Int. J. Dev. Neurosci.

    (1998)
  • B.S. McEwen et al.

    The concept of allostasis in biology and biomedicine

    Horm. Behav.

    (2003)
  • B.S. McEwen et al.

    What is in a name? Integrating homeostasis, allostasis and stress

    Horm. Behav.

    (2010)
  • J.J. Millspaugh et al.

    Use of fecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation

    Gen. Comp. Endocrinol.

    (2004)
  • L.M. Romero

    Physiological stress in ecology: lessons from biomedical research

    Trends Ecol. Evol.

    (2004)
  • L.M. Romero et al.

    Neurally-active stress peptide inhibits territorial defense in wild birds

    Horm. Behav.

    (1998)
  • L.M. Romero et al.

    The reactive scope model – a new model integrating homeostasis, allostasis, and stress

    Horm. Behav.

    (2009)
  • L.M. Romero et al.

    Adrenocorticotropin secretagog release: stimulation by frustration and paradoxically by reward presentation

    Brain Res.

    (1995)
  • L.M. Romero et al.

    Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone

    Gen. Comp. Endocrinol.

    (2000)
  • R.A. Sarabdjitsingh et al.

    Glucocorticoid pulsatility and rapid corticosteroid actions in the central stress response

    Physiol. Behav.

    (2012)
  • T. Stohr et al.

    Lewis/fischer rat strain differences in endocrine and behavioural responses to environmental challenge

    Pharmacol. Biochem. Behav.

    (2000)
  • E.M. Tarlow et al.

    Evaluating methods to quantify anthropogenic stressors on wild animals

    Appl. Anim. Behav. Sci.

    (2007)
  • K. Ushijima et al.

    Chronobiological disturbances with hyperthermia and hypercortisolism induced by chronic mild stress in rats

    Behav. Brain Res.

    (2006)
  • M. Wikelski et al.

    Conservation physiology

    Trends Ecol. Evol.

    (2006)
  • M. Wikgren et al.

    Short telomeres in depression and the general population are associated with a hypocortisolemic state

    Biol. Psychiatry

    (2012)
  • H.A.H. Wu et al.

    Strain differences in the chronic mild stress animal model of depression

    Behav. Brain Res.

    (2010)
  • Aguirre, A.A., 2009. Wild canids as sentinels of ecological health: A conservation medicine perspective, Parasites and...
  • R. Arlettaz et al.

    Spreading free-riding snow sports represent a novel serious threat for wildlife

    Proc. R. Soc. B: Biol. Sci.

    (2007)
  • Cited by (376)

    • Investigating the effects of acute and chronic stress on DNA damage

      2024, Journal of Experimental Zoology Part A: Ecological and Integrative Physiology
    View all citing articles on Scopus
    View full text