Review of factors influencing stress hormones in fish and wildlife

Abstract

Conservation efforts to better understand how wildlife populations respond to environmental change and anthropogenic disturbance has led to a proliferation of research examining physiological indicators of stress response in wildlife. Glucocorticoid stress hormones (GCs), typically cortisol and corticosterone, are among the most frequently measured indicators of the vertebrate stress response. To review the current state of research on stress physiology of free-ranging animals and its application to conservation, we canvassed more than 1000 articles on GC measures in wildlife published since 1969. For 454 studies published since 1990, we assessed the most commonly analysed correlates and disturbances and conducted a meta-analysis on commonly studied species. We noted a prominent divide in the legacies of fish-related analyses and those of higher order vertebrates and the need and opportunity to transfer knowledge between fields. Fish studies most frequently measured physiological indicators, condition, and the relationship between stress and mortality, whereas other vertebrate studies most frequently measured reproduction, condition, and environmental correlates. Correlates that significantly influenced GC levels across all vertebrate groups and are thus important to control for in study design and analyses include density and dispersal of conspecifics, season, reproductive status, and social status. Consistent trends across commonly studied species included positive GC response to capture and handling, reduced GC response related to acclimation, and a lack of correlation between condition and baseline GC levels. Our synthesis within and across diverse taxonomic orders reveals substantial research coverage but a lack of depth in multivariate analyses and a disparity in how correlates are controlled. This paper provides a comprehensive assessment of correlates and disturbances that influence GC measures and, as such, has useful applications to assist conservation physiologists in study design, analysis, and interpretation.

Introduction

Increased interest in understanding and predicting wildlife responses to environmental change and anthropogenic disturbance has resulted in an expansive body of research related to physiological indicators of stress in wildlife. While stress physiology represents a prominent and growing component of the field of conservation physiology (Wikelski & Cooke 2006), few analyses exist that synthesise trends and approaches. This manuscript provides a comprehensive assessment of correlates and disturbances that influence measures of stress physiology. It is designed to inform conservation physiologists, wildlife managers, and research scientists in the development of study design, data analysis and interpretation, and support ongoing efforts to improve management and monitoring of species of concern. The broad nature of this review provides important insights that may be lost in analyses focused on single species or taxa. This study also highlights important methodologies and findings from a broad range of disciplines and identifies areas for interdisciplinary synergies and exchange.

Wildlife and natural resource managers are increasingly tasked with providing concrete data on the health of fish and wildlife populations, determining cause and effect in species declines and determining causal mechanisms between disturbance and the persistence and health of affected populations. Conservationists, veterinarians, and regulators tasked with developing and monitoring environmental guidelines also must understand the effects of environmental disturbance on protected species, managed populations, and biological communities generally. The emerging field of conservation physiology links environmental change and ecological performance to provide a more mechanistic understanding of how environmental disturbances and external pressures influence the physiological function of individuals and, consequently, population persistence and ecological function (Seebacher & Franklin 2012). Physiological analyses, particularly measurements of physiological stress, have the potential to contribute to identifying and addressing complex challenges in wildlife conservation and management. Physiological research in wild populations provide essential baseline data, allow the monitoring of populations over time, enable the rapid assessment of various natural and anthropogenic pressures, elucidate causal mechanisms, and facilitate evaluation of the efficacy of targeted actions. While in the recent past most physiological measurements were conducted in controlled conditions, advances in biotelemetry and an increasing range of direct and noninvasive methods to measure physiological stress in the wild allows conservation physiologists to study free-ranging animals (Metcalfe et al. 2012). A growing number of research initiatives are applying these tools in natural settings to better understand the factors that influence and modulate stress responses in wild populations and place stress physiology in an ecologically relevant framework. Challenges remain, however, as the drivers of stress hormones are complex and highly context dependent. To properly assess field measurements, strict attention must be paid to how to control for confounding influences and interpret physiological metrics within the context of the natural environment.

The stress response may be defined as the functional response of an organism to an external stressor (Selye & Fortier 1950). Understanding and interpreting stress, its role, its positive and negative implications, and the mechanisms driving the stress response has developed heuristically over time (Barton, 2002, Levine, 1971, Levine and Ursin, 1991, Pickering, 1981, Selye, 1974). Generally, the stress response encompasses a suite of behavioural responses and physiological processes elicited by an organism to maintain a viable metabolic state when confronted with a physical or chemical challenge (Romero 2004). Acute responses to stressors may be beneficial in enabling an animal to surmount an immediate challenge. Chronic exposure to stressful conditions, however, often result in decreased performance or survival and incur costs that may be unsustainable over the long-term (Davis, 2006, Goymann and Wingfield, 2004).

The activation of the hypothalamic-pituitary-adrenal (HPA) axis and subsequent synthesis and release of glucocorticoids (GC) is central to the vertebrate stress response (Moberg & Mench 2000). Glucocorticoid (GC) hormones, typically cortisol and corticosterone are the most frequently measured indicators of stress in vertebrates (Wingfield et al. 1997). Both acute and chronic stress may incite GC release, which mobilises energy reserves via conversion of glycogen to energy rich glucose (Reeder & Kramer 2005). Glucocorticoids alter physiological processes facilitating necessary responses to physical challenge or adaptation to environmental change, allowing the organism to function beyond normal limitations. These biochemical and biophysical processes constitute an additional energy demand and may have deleterious effects. A short-term stress response to an acute, ephemeral stressor represents an adaptive ability to cope with the stimulus, prioritising immediate survival, while suspending long-term objectives such as energy storage, reproduction, and growth (Barton 2002). A chronic stress response to a persistent stressor, however, can be detrimental to the organism and result in compromised growth and condition, immunodeficiency, reproductive suppression, and reduced survival (Reeder and Kramer, 2005, Schreck, 2000).

Analysis of the stress response in wildlife has numerous applications to wildlife conservation and management (Wingfield et al. 1997). As a response variable, hormone levels offer important advantages to alternatives such as population growth rate, reproductive success measures, and behaviour (Mostl & Palme 2002). Hormones change rapidly in response to disturbance and thus represent a more sensitive measure than individual survivorship or population growth alone, with the ability to detect chronic, sub-lethal effects. Physiological analyses may also be more intelligible than analyses of behaviour. Hormonal response variables lend themselves well to experimental tests of disturbance in which impacts must be assessed in a relatively short timeframe (Breuner et al. 2008). GC hormone levels, in particular, rise in response to a range of perturbations and function as convenient, proximate indicators of potential decline in reproductive success and survivorship (Wingfield et al. 1997), fitness variables typically difficult to quantify in timeframes useful to inform conservation and management.

While physiological measures of stress offer great promise as measuring, monitoring, and predictive tools for conservation (Wingfield et al. 1997), both inherent and external correlates influence GC measures (Reeder & Kramer 2005) and may confound study results and their interpretation. Proper consideration of context and environment is necessary to facilitate effective measurement and monitoring of the health of wild populations and ensure GC measures serve as effective tools for conservation and management. Monitoring animals of conservation concern typically occurs in natural systems where not all variables can be overtly controlled. As a consequence, many potentially important variables are often omitted from analysis, which may contribute to ambiguous or conflicting trends in GC measures across taxa, habitats, and studies (Busch & Hayward 2009). Identifying, monitoring and analysing or controlling for relevant variables will strengthen inference and better position researchers to accurately characterise wildlife responses to management and disturbance.

Research on drivers influencing HPA activation, GC synthesis and release, and related physiological and behavioural processes are numerous (Keay et al., 2006, Pankhurst, 2011). We describe the current state of research concerned with stress physiology of wild animals by canvassing peer-reviewed journals for relevant articles published since 1969. We delineate the breadth of studies completed across vertebrate taxa and identify research gaps. We inventory and report the range of quantifiable biological and environmental correlates that were considered as potential influences on GC values. We inspect patterns of significance and interactions with respect to GCs and examine the consistency of these patterns across taxa and studies. We then use meta-analyses to examine the consistency of the stress response where measures are congruent.

Although the form and function of the stress hormones is highly similar across taxa (Moberg & Mench 2000), differences in habitat, life history, conservation concern and management focus have distinguished approaches in various disciplines. Both the context and the focus of research on stress physiology in fish differs from that of other vertebrate classes. Due to exploitation and the direct management of many fish populations, manipulation through harvests, hatcheries, and aquaculture, and their commercial importance (Barton and Iwama, 1991, Pankhurst, 2011), greater resources have been directed toward analyses of stress in fishes. This longer and more extensive history suggests insights from analyses in fish taxa may be valuable in directing research in other terrestrial organisms. Throughout these analyses, we highlight the divergent emphasis on the disciplines of aquatic and terrestrial taxa and compare and contrast the approach and findings across taxa to draw attention to important developments in each field and to identify important areas for synergy and constructive exchange.