Biological mechanisms matter in contemporary wildlife conservation.

Given limited resources for wildlife conservation paired with an urgency to halt declines and rebuild populations, it is imperative that management actions are tactical and effective. Mechanisms are about how a system works and can inform threat identification and mitigation such that conservation actions that work can be identified. Here, we call for a more mechanistic approach to wildlife conservation and management where behavioral and physiological tools and knowledge are used to characterize drivers of decline, identify environmental thresholds, reveal strategies that would restore populations, and prioritize conservation actions. With a growing toolbox for doing mechanistic conservation research as well as a suite of decision-support tools (e.g., mechanistic models), the time is now to fully embrace the concept that mechanisms matter in conservation ensuring that management actions are tactical and focus on actions that have the potential to directly benefit and restore wildlife populations.

Researcher perspectives on challenges and opportunities in conservation physiology revealed from an online survey.

Conservation physiology represents a recently emerging arm of conservation science that applies physiological tools and techniques to understand and solve conservation issues. While a multi-disciplinary toolbox can only help to address the global biodiversity crisis, any field can face challenges while becoming established, particularly highly applied disciplines that require multi-stakeholder involvement. Gaining first-hand knowledge of the challenges that conservation physiologists are facing can help characterize the current state of the field and build a better foundation for determining how it can grow. Through an online survey of 468 scientists working at the intersection of physiology and conservation, we aimed to identify characteristics of those engaging in conservation physiology research (e.g. demographics, primary taxa of study), gauge conservation physiology's role in contributing to on-the-ground conservation action, identify the perceived barriers to achieving success and determine how difficult any identified barriers are to overcome. Despite all participants having experience combining physiology and conservation, only one-third considered themselves to be 'conservation physiologists'. Moreover, there was a general perception that conservation physiology does not yet regularly lead to tangible conservation success. Respondents identified the recent conceptualization of the field and the broader issue of adequately translating science into management action as the primary reasons for these deficits. Other significant barriers that respondents have faced when integrating physiology and conservation science included a lack of funding, logistical constraints (e.g. sample sizes, obtaining permits) and a lack of physiological baseline data (i.e. reference ranges of a physiological metric's 'normal' or pre-environmental change levels). We identified 12 actions based on suggestions of survey participants that we anticipate will help deconstruct the barriers and continue to develop a narrative of physiology that is relevant to conservation science, policy and practice.

Exploiting common senses: sensory ecology meets wildlife conservation and management.

Multidisciplinary approaches to conservation and wildlife management are often effective in addressing complex, multi-factor problems. Emerging fields such as conservation physiology and conservation behaviour can provide innovative solutions and management strategies for target species and systems. Sensory ecology combines the study of 'how animals acquire' and process sensory stimuli from their environments, and the ecological and evolutionary significance of 'how animals respond' to this information. We review the benefits that sensory ecology can bring to wildlife conservation and management by discussing case studies across major taxa and sensory modalities. Conservation practices informed by a sensory ecology approach include the amelioration of sensory traps, control of invasive species, reduction of human-wildlife conflicts and relocation and establishment of new populations of endangered species. We illustrate that sensory ecology can facilitate the understanding of mechanistic ecological and physiological explanations underlying particular conservation issues and also can help develop innovative solutions to ameliorate conservation problems.

One hundred research questions in conservation physiology for generating actionable evidence to inform conservation policy and practice.

Environmental change and biodiversity loss are but two of the complex challenges facing conservation practitioners and policy makers. Relevant and robust scientific knowledge is critical for providing decision-makers with the actionable evidence needed to inform conservation decisions. In the Anthropocene, science that leads to meaningful improvements in biodiversity conservation, restoration and management is desperately needed. Conservation Physiology has emerged as a discipline that is well-positioned to identify the mechanisms underpinning population declines, predict responses to environmental change and test different in situ and ex situ conservation interventions for diverse taxa and ecosystems. Here we present a consensus list of 10 priority research themes. Within each theme we identify specific research questions (100 in total), answers to which will address conservation problems and should improve the management of biological resources. The themes frame a set of research questions related to the following: (i) adaptation and phenotypic plasticity; (ii) human-induced environmental change; (iii) human-wildlife interactions; (iv) invasive species; (v) methods, biomarkers and monitoring; (vi) policy, engagement and communication; (vii) pollution; (viii) restoration actions; (ix) threatened species; and (x) urban systems. The themes and questions will hopefully guide and inspire researchers while also helping to demonstrate to practitioners and policy makers the many ways in which physiology can help to support their decisions.

Conservation physiology and the COVID-19 pandemic.

The COVID-19 pandemic and associated public health measures have had unanticipated effects on ecosystems and biodiversity. Conservation physiology and its mechanistic underpinnings are well positioned to generate robust data to inform the extent to which the Anthropause has benefited biodiversity through alterations in disturbance-, pollution- and climate change-related emissions. The conservation physiology toolbox includes sensitive biomarkers and tools that can be used both retroactively (e.g. to reconstruct stress in wildlife before, during and after lockdown measures) and proactively (e.g. future viral waves) to understand the physiological consequences of the pandemic. The pandemic has also created new risks to ecosystems and biodiversity through extensive use of various antimicrobial products (e.g. hand cleansers, sprays) and plastic medical waste. Conservation physiology can be used to identify regulatory thresholds for those products. Moreover, given that COVID-19 is zoonotic, there is also opportunity for conservation physiologists to work closely with experts in conservation medicine and human health on strategies that will reduce the likelihood of future pandemics (e.g. what conditions enable disease development and pathogen transfer) while embracing the One Health concept. The conservation physiology community has also been impacted directly by COVID-19 with interruptions in research, training and networking (e.g. conferences). Because this is a nascent discipline, it will be particularly important to support early career researchers and ensure that there are recruitment pathways for the next generation of conservation physiologists while creating a diverse and inclusive community. We remain hopeful for the future and in particular the ability of the conservation physiology community to deliver relevant, solutions-oriented science to guide decision makers particularly during the important post-COVID transition and economic recovery.

Reframing conservation physiology to be more inclusive, integrative, relevant and forward-looking: reflections and a horizon scan.

Applying physiological tools, knowledge and concepts to understand conservation problems (i.e. conservation physiology) has become commonplace and confers an ability to understand mechanistic processes, develop predictive models and identify cause-and-effect relationships. Conservation physiology is making contributions to conservation solutions; the number of 'success stories' is growing, but there remain unexplored opportunities for which conservation physiology shows immense promise and has the potential to contribute to major advances in protecting and restoring biodiversity. Here, we consider how conservation physiology has evolved with a focus on reframing the discipline to be more inclusive and integrative. Using a 'horizon scan', we further explore ways in which conservation physiology can be more relevant to pressing conservation issues of today (e.g. addressing the Sustainable Development Goals; delivering science to support the UN Decade on Ecosystem Restoration), as well as more forward-looking to inform emerging issues and policies for tomorrow. Our horizon scan provides evidence that, as the discipline of conservation physiology continues to mature, it provides a wealth of opportunities to promote integration, inclusivity and forward-thinking goals that contribute to achieving conservation gains. To advance environmental management and ecosystem restoration, we need to ensure that the underlying science (such as that generated by conservation physiology) is relevant with accompanying messaging that is straightforward and accessible to end users.

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.

The conservation physiology toolbox: status and opportunities.

For over a century, physiological tools and techniques have been allowing researchers to characterize how organisms respond to changes in their natural environment and how they interact with human activities or infrastructure. Over time, many of these techniques have become part of the conservation physiology toolbox, which is used to monitor, predict, conserve, and restore plant and animal populations under threat. Here, we provide a summary of the tools that currently comprise the conservation physiology toolbox. By assessing patterns in articles that have been published in 'Conservation Physiology' over the past 5 years that focus on introducing, refining and validating tools, we provide an overview of where researchers are placing emphasis in terms of taxa and physiological sub-disciplines. Although there is certainly diversity across the toolbox, metrics of stress physiology (particularly glucocorticoids) and studies focusing on mammals have garnered the greatest attention, with both comprising the majority of publications (>45%). We also summarize the types of validations that are actively being completed, including those related to logistics (sample collection, storage and processing), interpretation of variation in physiological traits and relevance for conservation science. Finally, we provide recommendations for future tool refinement, with suggestions for: (i) improving our understanding of the applicability of glucocorticoid physiology; (ii) linking multiple physiological and non-physiological tools; (iii) establishing a framework for plant conservation physiology; (iv) assessing links between environmental disturbance, physiology and fitness; (v) appreciating opportunities for validations in under-represented taxa; and (vi) emphasizing tool validation as a core component of research programmes. Overall, we are confident that conservation physiology will continue to increase its applicability to more taxa, develop more non-invasive techniques, delineate where limitations exist, and identify the contexts necessary for interpretation in captivity and the wild.

Conservation physiology and the quest for a 'good' Anthropocene.

It has been proposed that we are now living in a new geological epoch known as the Anthropocene, which is specifically defined by the impacts that humans are having on the Earth's biological diversity and geology. Although the proposal of this term was borne out of an acknowledgement of the negative changes we are imparting on the globe (e.g. climate change, pollution, coastal erosion, species extinctions), there has recently been action amongst a variety of disciplines aimed at achieving a 'good Anthropocene' that strives to balance societal needs and the preservation of the natural world. Here, we outline ways that the discipline of conservation physiology can help to delineate a hopeful, progressive and productive path for conservation in the Anthropocene and, specifically, achieve that vision. We focus on four primary ways that conservation physiology can contribute, as follows: (i) building a proactive approach to conservation; (ii) encouraging a pragmatic perspective; (iii) establishing an appreciation for environmental resilience; and (iv) informing and engaging the public and political arenas. As a collection of passionate individuals combining theory, technological advances, public engagement and a dedication to achieving conservation success, conservation physiologists are poised to make meaningful contributions to the productive, motivational and positive way forward that is necessary to curb and reverse negative human impact on the environment.

An evaluation of feather corticosterone as a biomarker of fitness and an ecologically relevant stressor during breeding in the wild.

Feather corticosterone (CORT) levels are increasingly employed as biomarkers of environmental stress. However, it is unclear if feather CORT levels reflect stress and/or workload in the wild. We investigated whether feather CORT represents a biomarker of environmental stress and reproductive effort in tree swallows (Tachycineta bicolor). Specifically, we examined whether individual state and investment during reproduction could predict feather CORT levels in subsequently moulted feathers and whether those levels could predict future survival and reproductive success. Through a manipulation of flight cost during breeding, we also investigated whether an increase in stress level would be reflected in subsequently grown feathers, and whether those levels could predict future success. We found that CORT levels of feathers grown during moult did not (1) reflect past breeding experience (n = 29), (2) predict reproductive output (n = 18), or (3) respond to a manipulation of flight effort during reproduction (10 experimental, 14 control females). While higher feather CORT levels predicted higher return rate (a proxy for survival), they did so only in the manipulated group (n = 36), and this relationship was opposite to expected. Overall, our results add to the mixed literature reporting that feather CORT levels can be positively, negatively, or not related to proxies of within-season and longer-term fitness (i.e., carryover effects). In addition, our results indicate that CORT levels or disturbances experienced during one time (e.g., breeding) may not carry over to subsequent stages (e.g., moult). We, therefore, petition for directed research investigating whether feather CORT represents exposure to chronic stress in feathers grown during moult.

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.

The measurement of corticosterone (CORT) levels in feathers has recently become an appealing tool for the conservation toolbox, potentially providing a non-invasive, integrated measure of stress activity throughout the time of feather growth. However, because the mechanism of CORT deposition, storage and stability in feathers is not fully understood, it is unclear how reliable this measure may be, especially when there is an extended interval between growth and feather collection. We compared CORT levels of naturally grown feathers from tree swallows (Tachycineta bicolor) that were moulted and regrown concurrently and therefore expected to have similar CORT levels. Specifically, we compared the same feather from the left and right wing (moulted symmetrically) and different types of feathers (wing, back and tail) expected to have been moulted within the same time period. We found that larger, heavier feathers held more CORT per unit length. In addition, we found a lack of concordance in CORT levels both within the same feather type and between different feather types, even after taking into account differences in feather density. Our results indicate that naturally grown feathers may not consistently provide an indication of stress status. Additionally, conflict in results may arise depending on the feather assayed, and total feather volume may be an important consideration when interpreting feather CORT levels. Future work is necessary to determine explicitly the mechanisms of CORT deposition, the effects of environmental exposure and feather wear on the permanence of the feather CORT signal, and the influence of responses to wild stressors on feather CORT levels, before feather CORT can be implemented effectively as a tool for ecological and conservation applications.

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

Labile physiological variables, such as stress hormones [i.e. glucocorticoids (GCs)], allow individuals to react to perturbations in their environment and may therefore reflect the effect of disturbances or positive conservation initiatives in advance of population-level demographic measures. Although the application of GCs as conservation biomarkers has been of extensive interest, few studies have explicitly investigated whether baseline GC concentrations respond to disturbances consistently across individuals. However, confirmation of consistent responses is of paramount importance to assessing the ease of use of GCs in natural systems and to making valid interpretations regarding population-level change (or lack of change) in GC concentrations. We investigated whether free-ranging female tree swallows (Tachycineta bicolor) display individually specific changes in baseline glucocorticoid concentrations naturally over the breeding season (from incubation to offspring provisioning) and in response to a manipulation of foraging profitability (representing a decrease in access to food resources). We show that baseline GC concentrations are repeatable within individuals over reproduction in natural conditions. However, in response to a reduction in foraging ability, baseline GC concentrations increase at the population level but are not repeatable within individuals, indicating a high level of within-individual variation. Overall, we suggest that baseline GCs measured on a subset of individuals may not provide a representative indication of responses to environmental change at the population level, and multiple within-individual measures may be necessary to determine the fitness correlates of GC concentrations. Further validation should be completed across a variety of taxa and life-history stages. Moving beyond a traditional cross-sectional approach by incorporating repeated-measures methods will be necessary to assess the suitability of baseline GCs as biomarkers of environmental change and population persistence, particularly from a logistical and ease-of-use perspective for conservation managers.

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.

Success stories and emerging themes in conservation physiology.

The potential benefits of physiology for conservation are well established and include greater specificity of management techniques, determination of cause-effect relationships, increased sensitivity of health and disturbance monitoring and greater capacity for predicting future change. While descriptions of the specific avenues in which conservation and physiology can be integrated are readily available and important to the continuing expansion of the discipline of 'conservation physiology', to date there has been no assessment of how the field has specifically contributed to conservation success. However, the goal of conservation physiology is to foster conservation solutions and it is therefore important to assess whether physiological approaches contribute to downstream conservation outcomes and management decisions. Here, we present eight areas of conservation concern, ranging from chemical contamination to invasive species to ecotourism, where physiological approaches have led to beneficial changes in human behaviour, management or policy. We also discuss the shared characteristics of these successes, identifying emerging themes in the discipline. Specifically, we conclude that conservation physiology: (i) goes beyond documenting change to provide solutions; (ii) offers a diversity of physiological metrics beyond glucocorticoids (stress hormones); (iii) includes approaches that are transferable among species, locations and times; (iv) simultaneously allows for human use and benefits to wildlife; and (v) is characterized by successes that can be difficult to find in the primary literature. Overall, we submit that the field of conservation physiology has a strong foundation of achievements characterized by a diversity of conservation issues, taxa, physiological traits, ecosystem types and spatial scales. We hope that these concrete successes will encourage the continued evolution and use of physiological tools within conservation-based research and management plans.

The Power of Physiology in Changing Landscapes: Considerations for the Continued Integration of Conservation and Physiology.

The growing field of conservation physiology applies a diversity of physiological traits (e.g., immunological, metabolic, endocrine, and nutritional traits) to understand and predict organismal, population, and ecosystem responses to environmental change and stressors. Although the discipline of conservation physiology is gaining momentum, there is still a pressing need to better translate knowledge from physiology into real-world tools. The goal of this symposium, ''Physiology in Changing Landscapes: An Integrative Perspective for Conservation Biology'', was to highlight that many current investigations in ecological, evolutionary, and comparative physiology are necessary for understanding the applicability of physiological measures for conservation goals, particularly in the context of monitoring and predicting the health, condition, persistence, and distribution of populations in the face of environmental change. Here, we outline five major investigations common to environmental and ecological physiology that can contribute directly to the progression of the field of conservation physiology: (1) combining multiple measures of physiology and behavior; (2) employing studies of dose­responses and gradients; (3) combining a within-individual and population-level approach; (4) taking into account the context-dependency of physiological traits; and (5) linking physiological variables with fitness metrics. Overall, integrative physiologists have detailed knowledge of the physiological systems that they study; however, communicating theoretical and empirical knowledge to conservation biologists and practitioners in an approachable and applicable way is paramount to the practical development of physiological tools that will have a tangible impact for conservation.