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Journal ArticleDOI

Reality as the leading cause of stress: rethinking the impact of chronic stress in nature

01 Feb 2013-Functional Ecology (Wiley/Blackwell (10.1111))-Vol. 27, Iss: 1, pp 11-23
TL;DR: It is proposed that chronic stress evolves in a species only if it is adaptive, with the key factors being lifespan and life history.
Abstract: Summary Chronic activation of the stress axis caused by long-term uncontrollable and unpredictable factors in the environment has been regarded as causing maladaptive and/or pathological effects, both by those studying animals in the laboratory and in nature. While pathology may apply to the former, I argue that it does not apply to the latter. Our thinking on the role of chronic stress in animals in nature has been heavily influenced by biomedical research, but much less so by the ecological and evolutionary context within which animals actually function. I argue that when such stressors occur (e.g. periods of high predation risk, food limitation, prolonged severe weather, social conflict, etc.), although the animal may be chronically stressed, its responses are adaptive and continue to promote fitness. Chronic stressors in nature can be subdivided into whether they are reactive (direct physiological challenges threatening homeostasis and not requiring cognitive processing – for example, food limitation) or anticipatory (perceived to be threatening and requiring cognitive processing – for example, high predation risk). For anticipatory stressors, their impact on the animal should not be based on their absolute duration (they may be acute), but rather by the duration of their physiological consequences. The anticipatory stressor of persistent high predation risk does not elicit chronic stress in all prey classes. Cyclic snowshoe hare and arctic ground squirrels exhibit evidence of chronic stress when predator numbers are high, but cyclic vole and noncyclic elk populations do not. I suggest that chronic stress has evolved to benefit the fitness of the former and not the later, with the key factors being lifespan and life history. I propose that chronic stress evolves in a species only if it is adaptive.
Citations
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Journal ArticleDOI
07 Jun 2013-Science
TL;DR: It is shown that exposing mothers to high-density cues, accomplished via playbacks of territorial vocalizations, led to increased offspring growth rates in the absence of additional food resources, and females with naturally or experimentally increased glucocorticoids produced offspring that grew faster than controls.
Abstract: In fluctuating environments, mothers may enhance the fitness of their offspring by adjusting offspring phenotypes to match the environment they will experience at independence. In free-ranging red squirrels, natural selection on offspring postnatal growth rates varies according to population density, with selection favoring faster-growing offspring under high-density conditions. We show that exposing mothers to high-density cues, accomplished via playbacks of territorial vocalizations, led to increased offspring growth rates in the absence of additional food resources. Experimental elevation of actual and perceived density induced higher maternal glucocorticoid levels, and females with naturally or experimentally increased glucocorticoids produced offspring that grew faster than controls. Therefore, social cues reflecting population density were sufficient to elicit increased offspring growth through an adaptive hormone-mediated maternal effect.

358 citations

Journal ArticleDOI
TL;DR: A meta-analysis shows that human activities consistently increase stress hormone levels across vertebrates, and five questions should be considered about the use of stress hormone measurements in conservation physiology are discussed.
Abstract: Conservation physiology proposes that measures of physiological stress (glucocorticoid levels) can be used to assess the status and future fate of natural populations. Increases in glucocorticoids may reflect a more challenging environment, suggesting that the influence of human activities on free-living animals could be quantified by measuring glucocorticoids. Biomedical studies suggest that chronic increases in glucocorticoids can have detrimental effects on survival and reproduction, which could influence the viability of populations. Here, we discuss the use of measurements of glucocorticoids in conservation physiology. We first provide an overview of the different methods to quantify glucocorticoids and their utility in conservation physiology. We then discuss five questions we think are essential for conservation physiologists to address. We highlight how intrinsic (e.g. sex, reproductive status, age, recent experiences) and ecological factors (e.g. predation, food availability, snowfall) can, by themselves or through their interactions with anthropogenic disturbances, affect the physiological stress response and mask any general patterns about the effects of anthropogenic disturbances on glucocorticoids. Using a meta-analysis, we show that anthropogenic disturbances are consistently associated with increased glucocorticoids regardless of the type of human disturbance. We also show that males may be more sensitive to anthropogenic disturbances than females and that faecal glucocorticoids, but not baseline plasma glucocorticoids, consistently increase in response to anthropogenic disturbances. Finally, we discuss how increases in glucocorticoids in free-living animals can sometimes enhance survival and reproduction. Unfortunately, our literature analysis indicates that this observation has not yet gained traction, and very few studies have shown that increases in glucocorticoid levels resulting from anthropogenic disturbances decrease survival or reproduction. We think that the use of measures of glucocorticoids in conservation physiology has tremendous potential, but there are still a number of methodological concerns, in addition to several crucial questions that should be addressed.

325 citations


Cites background from "Reality as the leading cause of str..."

  • ...Until recently, most physiological ecologists working on natural populations have accepted this traditional view (Boonstra, 2013)....

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  • ...Chronic or long-term increases in glucocorticoid levels, however, are widely touted as having detrimental effects, though the evidence comes largely from biomedical studies in humans or laboratory animals (Romero, 2004; Korte et al., 2005; Boonstra, 2013)....

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Book ChapterDOI
TL;DR: Fish physiology has progressed to the point where it can easily recognize when fish are stressed, but it cannot always recognize when Fish are unstressed because the lack of clinical signs of stress does not always correspond to fish being unstressed, so fish scientists need to be aware of the possibility of false negatives regarding clinical Signs of stress.
Abstract: 1. Introduction 1.1. What Is Stress? 1.2. Dynamics of the Stress Response and Effects on Performance 1.3. Contemporary View of the GAS: Eustress versus Distress 1.4. Sensory Systems and Perception 1.5. Adaptation versus Nonadaptation Aspects of the Stress Response 1.6. Key Unknowns The general physiological response of fish to threatening situations, as with all vertebrates, is referred to as stress. A stress response is initiated almost immediately following the perception of a stressor. Mildly stressful situations can have beneficial or positive effects (eustress), while higher severities induce adaptive responses but also can have maladaptive or negative consequences (distress). The stress response is initiated and controlled by two hormonal systems, those leading to the production of corticosteroids (mainly cortisol) and catecholamines (such as adrenaline and noradrenaline and their precursor dopamine). Together these regulate the secondary stress response factors that alter the distribution of necessary resources such as energy sources and oxygen to vital areas of the body, as well as compromise hydromineral imbalance and the immune system. If fish can resist death due to a stressor, they recover to a similar or somewhat similar homeostatic norm. Long-term consequences of repeated or prolonged exposures to stress are maladaptive by negatively affecting other necessary life functions (growth, development, disease resistance, behavior, and reproduction), in large part because of the energetic cost associated with mounting the stress response (allostatic load). There is considerable variation in how fish respond to a stressor because of genetic differences among different taxa and also within stocks and species. Variations within the stress response are introduced by the environmental history of the fish, present ambient environmental conditions, and the fish's present physiological condition. Currently, fish physiology has progressed to the point where we can easily recognize when fish are stressed, but we cannot always recognize when fish are unstressed because the lack of clinical signs of stress does not always correspond to fish being unstressed. In other words, we need to be aware of the possibility of false negatives regarding clinical signs of stress. In addition, we cannot use clinical data to precisely or accurately infer severity of a stressor.

278 citations

01 Jan 2014
TL;DR: The use of measurements of glucocorticoids in conservation physiology has been discussed in this paper, where the authors show that anthropogenic disturbances are consistently associated with increased glucoc corticoid levels regardless of the type of human disturbance.
Abstract: Conservation physiology proposes that measures of physiological stress (glucocorticoid levels) can be used to assess the status and future fate of natural populations. Increases in glucocorticoids may reflect a more challenging environment, suggest ing that the influence of human activities on free-living animals could be quantified by measuring glucocorticoids. Biomedical studies suggest that chronic increases in glucocorticoids can have detrimental effects on survival and reproduction, which could influence the viability of populations. Here, we discuss the use of measurements of glucocorticoids in conservation physiology. We first provide an overview of the different methods to quantify glucocorticoids and their utility in conservation physiology. We then discuss five questions we think are essential for conservation physiologists to address. We highlight how intrinsic (e.g. sex, reproductive status, age, recent experiences) and ecological factors (e.g. predation, food availability, snowfall) can, by themselves or through their interactions with anthropogenic disturbances, affect the physiological stress response and mask any general patterns about the effects of anthropogenic disturbances on glucocorticoids. Using a meta-analysis, we show that anthropogenic disturbances are consistently associated with increased glucocorticoids regardless of the type of human disturbance. We also show that males may be more sensitive to anthropogenic disturbances than females and that faecal glucocorticoids, but not baseline plasma glucocorticoids, consistently increase in response to anthropogenic disturbances. Finally, we discuss how increases in glucocorticoids in free-living animals can sometimes enhance survival and reproduction. Unfortunately, our literature analysis indicates that this observation has not yet gained traction, and very few studies have shown that increases in glucocorticoid levels resulting from anthropogenic disturbances decrease survival or reproduction. We think that the use of measures of glucocorticoids in conservation physiology has tremendous potential, but there are still a number of methodological concerns, in addition to several crucial questions that should be addressed.

250 citations

Journal ArticleDOI
TL;DR: It is suggested that viewing stressors as environmental changes that cause reductions in performance or fitness provides the broadest and most useful conception of the phenomenon of stress.
Abstract: Although the term environmental stress is used across multiple fields in biology, the inherent ambiguity associated with its definition has caused confusion when attempting to understand organismal responses to environmental change. Here I provide a brief summary of existing definitions of the term stress, and the related concepts of homeostasis and allostasis, and attempt to unify them to develop a general framework for understanding how organisms respond to environmental stressors. I suggest that viewing stressors as environmental changes that cause reductions in performance or fitness provides the broadest and most useful conception of the phenomenon of stress. I examine this framework in the context of animals that have evolved in highly variable environments, using the Atlantic killifish, Fundulus heteroclitus, as a case study. Consistent with the extreme environmental variation that they experience in their salt marsh habitats, killifish have substantial capacity for both short-term resistance and long-term plasticity in the face of changing temperature, salinity and oxygenation. There is inter-population variation in the sensitivity of killifish to environmental stressors, and in their ability to acclimate, suggesting that local adaptation can shape the stress response even in organisms that are broadly tolerant and highly plastic. Whole-organism differences between populations in stressor sensitivity and phenotypic plasticity are reflected at the biochemical and molecular levels in killifish, emphasizing the integrative nature of the response to environmental stressors. Examination of this empirical example highlights the utility of using an evolutionary perspective on stressors, stress and stress responses.

244 citations


Cites background from "Reality as the leading cause of str..."

  • ...Some have questioned whether type II allostasic overload ever occurs in nature or whether it is strictly a laboratory phenomenon (Boonstra, 2013), but putting these specific issues aside, the concept of allostatic load focuses us on the key issue of the costs of mounting a response to an environmental change, and the importance of distinguishing between responses that are beneficial, those that may impose a significant cost and those that may actually cause harm....

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  • ...Much of this confusion may stem from the fact that stress research has developed relatively independently across several fields of biology, with substantial gulfs between those interested in stress from a biomedical perspective and those interested in the effects of stressors in natural populations (Bijlsma and Loeschcke, 2005; Boonstra, 2013)....

    [...]

  • ...…stress research has developed relatively independently across several fields of biology, with substantial gulfs between those interested in stress from a biomedical perspective and those interested in the effects of stressors in natural populations (Bijlsma and Loeschcke, 2005; Boonstra, 2013)....

    [...]

  • ...Some have questioned whether type II allostasic overload ever occurs in nature or whether it is strictly a laboratory phenomenon (Boonstra, 2013), but putting these specific issues aside, the concept of allostatic load focuses us on the key issue of the costs of mounting a response to an…...

    [...]

References
More filters
Journal ArticleDOI
TL;DR: This review considers recent findings regarding GC action and generates criteria for determining whether a particular GC action permits, stimulates, or suppresses an ongoing stress-response or, as an additional category, is preparative for a subsequent stressor.
Abstract: The secretion of glucocorticoids (GCs) is a classic endocrine response to stress. Despite that, it remains controversial as to what purpose GCs serve at such times. One view, stretching back to the time of Hans Selye, posits that GCs help mediate the ongoing or pending stress response, either via basal levels of GCs permitting other facets of the stress response to emerge efficaciously, and/or by stress levels of GCs actively stimulating the stress response. In contrast, a revisionist viewpoint posits that GCs suppress the stress response, preventing it from being pathologically overactivated. In this review, we consider recent findings regarding GC action and, based on them, generate criteria for determining whether a particular GC action permits, stimulates, or suppresses an ongoing stressresponse or, as an additional category, is preparative for a subsequent stressor. We apply these GC actions to the realms of cardiovascular function, fluid volume and hemorrhage, immunity and inflammation, metabolism, neurobiology, and reproductive physiology. We find that GC actions fall into markedly different categories, depending on the physiological endpoint in question, with evidence for mediating effects in some cases, and suppressive or preparative in others. We then attempt to assimilate these heterogeneous GC actions into a physiological whole. (Endocrine Reviews 21: 55‐ 89, 2000)

6,707 citations

Journal ArticleDOI
TL;DR: The relationship of allostatic load to genetic and developmental predispositions to disease is considered and examples will be given from research pertaining to autonomic, CNS, neuroendocrine, and immune system activity.
Abstract: Adaptation in the face of potentially stressful challenges involves activation of neural, neuroendocrine and neuroendocrine-immune mechanisms. This has been called "allostasis" or "stability through change" by Sterling and Eyer (Fisher S., Reason J. (eds): Handbook of Life Stress, Cognition and Health. J. Wiley Ltd. 1988, p. 631), and allostasis is an essential component of maintaining homeostasis. When these adaptive systems are turned on and turned off again efficiently and not too frequently, the body is able to cope effectively with challenges that it might not otherwise survive. However, there are a number of circumstances in which allostatic systems may either be overstimulated or not perform normally, and this condition has been termed "allostatic load" or the price of adaptation (McEwen and Stellar, Arch. Int. Med. 1993; 153: 2093.). Allostatic load can lead to disease over long periods. Types of allostatic load include (1) frequent activation of allostatic systems; (2) failure to shut off allostatic activity after stress; (3) inadequate response of allostatic systems leading to elevated activity of other, normally counter-regulated allostatic systems after stress. Examples will be given for each type of allostatic load from research pertaining to autonomic, CNS, neuroendocrine, and immune system activity. The relationship of allostatic load to genetic and developmental predispositions to disease is also considered.

3,876 citations

Journal ArticleDOI
15 Jul 2011-Science
TL;DR: This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles.
Abstract: Until recently, large apex consumers were ubiquitous across the globe and had been for millions of years. The loss of these animals may be humankind's most pervasive influence on nature. Although such losses are widely viewed as an ethical and aesthetic problem, recent research reveals extensive cascading effects of their disappearance in marine, terrestrial, and freshwater ecosystems worldwide. This empirical work supports long-standing theory about the role of top-down forcing in ecosystems but also highlights the unanticipated impacts of trophic cascades on processes as diverse as the dynamics of disease, wildfire, carbon sequestration, invasive species, and biogeochemical cycles. These findings emphasize the urgent need for interdisciplinary research to forecast the effects of trophic downgrading on process, function, and resilience in global ecosystems.

3,130 citations

Journal ArticleDOI
TL;DR: The concept of allostasis is discussed, maintaining stability through change, as a fundamental process through which organisms actively adjust to both predictable and unpredictable events, using the balance between energy input and expenditure as the basis for applying the concept.

2,782 citations

Journal ArticleDOI
Andreas Arvidsson1, Tove Collin1, Deniz Kirik1, Zaal Kokaia1, Olle Lindvall1 
TL;DR: It is shown that stroke, caused by transient middle cerebral artery occlusion in adult rats, leads to a marked increase of cell proliferation in the subventricular zone, and stroke induces differentiation of new neurons into the phenotype of most of the neurons destroyed by the ischemic lesion.
Abstract: In the adult brain, new neurons are continuously generated in the subventricular zone and dentate gyrus, but it is unknown whether these neurons can replace those lost following damage or disease. Here we show that stroke, caused by transient middle cerebral artery occlusion in adult rats, leads to a marked increase of cell proliferation in the subventricular zone. Stroke-generated new neurons, as well as neuroblasts probably already formed before the insult, migrate into the severely damaged area of the striatum, where they express markers of developing and mature, striatal medium-sized spiny neurons. Thus, stroke induces differentiation of new neurons into the phenotype of most of the neurons destroyed by the ischemic lesion. Here we show that the adult brain has the capacity for self-repair after insults causing extensive neuronal death. If the new neurons are functional and their formation can be stimulated, a novel therapeutic strategy might be developed for stroke in humans.

2,763 citations