Christine L. Madliger

The Need for a Predictive, Context-Dependent Approach to the Application of Stress Hormones in Conservation

Monitoring the impact of anthropogenic disturbance on species or populations of interest is an important goal of conservation (Van Dyke 2008). Because the effects of environmental alteration often manifest in an organism’s physiology before changes can be detected at the population level, physiological measures can provide earlier detection of disturbances and greater predictive capacity than traditional demographic methods (Wikelski & Cooke 2006; Ellis et al. 2012). This mechanistic approach, known as conservation physiology, can also help determine which populations are most susceptible to disturbance, key periods when disturbances may be most detrimental, and whether management techniques are having positive effects (Carey 2005; Wikelski & Cooke 2006). Incorporating physiological biomarkers into population monitoring also provides the opportunity to interpret anthropogenic changes from the perspective of the organism rather than the researcher and thus improve our understanding of which conditions constitute a disturbance. Glucocorticoids (GCs), often referred to as stress hormones, represent some of the most widely proposed physiological biomarkers (Cooke & O’Connor 2010). GCs (e.g., corticosterone and cortisol) act in 2 distinct and separately measurable ways as determined by their circulating concentration and the receptors to which they bind (Landys et al. 2006). GCs are best known for their role in enabling individuals to respond to unpredictable events such as extreme weather, predator interaction, or social conflict through the acute stress response (McEwen & Wingfield 2003). By increasing within minutes of

Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird

Determining the mechanisms that mediate investment decisions between current and future reproductive attempts is still a key goal of life-history studies. Since baseline levels of stress hormones (glucocorticoids - GCs) act as predictive and labile regulators of daily energetic balance in vertebrates they remain excellent candidates for mediating investment decisions both within and across reproductive attempts. Using free-living female European starlings (Sturnus vulgaris) we experimentally reduced investment in current reproduction (number of offspring raised in the first brood) to examine whether baseline corticosterone (CORT) acted as a hormonal mediator preparing individuals for a predictable increase in future investment (number of offspring raised in the second brood). Although treatment and control birds raised the same total amount of offspring across two broods, the experimental birds increased reproductive investment in second broods to compensate for the reduced investment in the first brood. Data on both mean and intra-individual changes in baseline CORT support the idea that an increase in baseline CORT between the incubation stages in treatment birds strongly predicted this increase in investment. Importantly, we measured the increase in baseline CORT during late incubation prior to the increase in energetic demand associated with increased reproductive investment in offspring, indicating that flexible within-individual changes in baseline GCs can act as a labile mechanism preparing individuals for predictable increases in reproductive investment. As such, our experimental results indicate that elevated baseline GCs can prepare individuals for investment in energetically expensive life-history stages, rather than simply being elevated as a consequence of increased effort or demand. This suggests that short-term preparative increases in baseline GCs benefit individuals by successfully allowing them to maximize fitness under varying environmental conditions.

Success stories and emerging themes in conservation physiology

The potential benefits of a physiological approach to conservation are well-established. Here we present a cross-section of conservation physiology success stories and a discussion of their shared characteristics to illustrate how the discipline has tangibly contributed to conservation and management across a diversity of topics, taxa, and spatial scales.

Toward improved conservation management: a consideration of sensory ecology

All organisms rely on sensory systems to obtain, interpret, and respond to information available in their environment. With rapid alterations of ecosystems occurring across the globe, organisms are being faced with sensory challenges that result in behavioural changes and disruptions with potential population-level consequences. Through a consideration of sensory ecology, it is possible to identify the underlying causes of disturbances at the individual level and use this information to develop better-informed, highly targeted, and more effective management strategies. Indeed, sensory-based approaches have already been successful in response to a variety of conservation issues. This article provides a general discussion of how a consideration of sensory ecology can benefit conservation biology and proceeds to describe three areas of rapid growth and potential for expansion: (1) mitigation of anthropogenic noise disturbance; (2) prevention and amelioration of ecological and other evolutionary traps; (3) targeted population control with special attention to aquatic invasive species. I conclude with general recommendations on how sensory ecologists and conservation biologists can mutually benefit from integrated endeavours.

Effectiveness of baseline corticosterone as a monitoring tool for fitness: a meta-analysis in seabirds

Many ecosystems have experienced anthropogenically induced changes in biodiversity, yet predicting these patterns has been difficult. Recently, individual behavioural and physiological measures have been proposed as more rapid links between environmental variation and fitness compared to demographics. Glucocorticoid hormones have received much attention given that they mediate energetic demands, metabolism, and foraging behaviour. However, it is currently unclear whether glucocorticoids can reliably predict environmental and fitness-related traits and whether they may be useful in specific groups of taxa. In particular, seabirds are a well-studied avian group often employed as biomonitoring tools for environmental change given their wide distribution and reliance on large oceanic patterns. Despite the increase in studies attempting to link variation in baseline corticosterone (the primary avian glucocorticoid) to variation in fitness-related traits in seabirds, there has been no comprehensive review of the relationship in this taxon. We present a phylogenetically controlled systematic review and meta-analysis of correlative and experimental studies examining baseline corticosterone as a predictor of fitness-related traits relevant to predicting seabird population health. Our results suggest that, while variation in baseline corticosterone may be a useful predictor of larger-scale environmental traits such as overall food availability and fitness-related traits such as reproductive success, this hormone may not be sensitive enough to detect variation in body condition, foraging effort, and breeding effort. Overall, our results support recent work suggesting that the use of baseline glucocorticoids as conservation biomarkers is complex and highly context dependent, and we suggest caution in their use and interpretation as simplified, direct biomarkers of fitness.

Temporal overlap and repeatability of feather corticosterone levels: practical considerations for use as a biomarker

We evaluated whether feather corticosterone represents a straightforward indicator of stress in birds by investigating the consistency of levels extracted from multiple tree swallow feathers grown at the same time but at different body locations. We found that different feathers contained different levels, complicating categorization of low- and high-stress individuals.

Employing individual measures of baseline glucocorticoids as population-level conservation biomarkers: considering within-individual variation in a breeding passerine

We outline the importance of considering within-individual changes in physiology when determining how disturbances may impact wildlife. Our results indicate that stress hormones measured on a subset of individuals may not provide a clear picture of how entire populations could respond to environmental change; multiple measures from the same individuals over time may be necessary.

Conservation implications of a lack of relationship between baseline glucocorticoids and fitness in a wild passerine

The application of physiological measures to conservation monitoring has been gaining momentum and, while a suite of physiological traits are available to ascertain disturbance and condition in wildlife populations, glucocorticoids (i.e., GCs; cortisol and corticosterone) are the most heavily employed. The interpretation of GC levels as sensitive indicators of population change necessitates that GCs and metrics of population persistence are linked. However, the relationship between GCs and fitness may be highly context-dependent, changing direction, or significance, depending on the GC measure, fitness metric, life history stage, or other intrinsic and extrinsic contexts considered. We examined the relationship between baseline plasma corticosterone (CORT) levels measured at two periods of the breeding season and three metrics of fitness (offspring quality, reproductive output, and adult survival) in female Tree Swallows (Tachycineta bicolor). Specifically, we investigated whether (1) a relationship between baseline CORT metrics and fitness exists in our population, (2) whether the inclusion of energetic contexts, such as food availability, reproductive investment, or body mass, could alter or improve the strength of the relationship between CORT and fitness, and (3) whether energetic contexts could better predict fitness compared to CORT metrics. Importantly, we investigated these relationships in both natural conditions and under an experimental manipulation of foraging profitability (feather clipping) to determine the influence of an environmental constraint on GC-fitness relationships. We found a lack of relationship between baseline CORT and both short- and long-term metrics of fitness in control and clipped birds. In contrast, loss in body mass over reproduction positively predicted reproductive output (number of chicks leaving the nest) in control birds; however, the relationship was characterized by a low R2 (5%), limiting the predictive capacity, and therefore the application potential, of such a measure in a conservation setting. Our results stress the importance of ground-truthing GC-fitness relationships and indicate that baseline GCs will likely not be easily employed as conservation biomarkers across some species and life history stages. Given the accumulating evidence of temporally dynamic, inconsistent, and context-dependent GC-fitness relationships, placing effort towards directly measuring fitness traits, rather than plasma GC levels, will likely be more worthwhile for many conservation endeavours.

Baseline corticosterone does not reflect iridescent plumage traits in female tree swallows

The production of high quality secondary sexual traits can be constrained by trade-offs in the allocation of energy and nutrients with other metabolic activities, and is mediated by physiological processes. In birds, the factors influencing male plumage quality have been well studied; however, factors affecting female plumage quality are poorly understood. Furthermore, it remains uncertain which physiological traits mediate the relationship between body condition and ornaments. In this three-year study of after-second-year female tree swallows (Tachycineta bicolor), we investigated (1) the relationship between baseline corticosterone near the end of the brood-rearing period (CORTBR) and feather colour characteristics (hue, saturation, brightness) the following year, and (2) the relationship between baseline corticosterone measured during incubation (CORTI) and brood rearing (CORTBR), and feather colour in the same year. To control for reproductive effort, we included reproductive parameters as covariates in all analyses. In this first study between CORT and the plumage colour characteristics of a species bearing iridescent feathers, we did not find any relationship between CORTBR and the colour of subsequently-produced feathers, nor did we find any relationship between CORT and the colour of feathers displayed during that breeding season. If CORT levels at the end of breeding carry over to influence the immediately subsequent moult period as we expect, our results generally indicate that structural plumage quality may not be as sensitive to circulating CORT levels compared to carotenoid-based colouration. Future studies, particularly those employing experimental manipulations of CORT during moult in species with iridescent traits, are necessary to fully determine the role glucocorticoids play in mediating the quality of secondary sexual characteristics.