Among-individual variation in thermal plasticity of fish metabolic rates causes profound variation in temperature-specific trait repeatability, but does not co-vary with behavioural plasticity.

Conspecifics of the same age and size differ consistently in the pace with which they expend energy. This among-individual variation in metabolic rate is thought to influence behavioural variation, since differences in energy requirements should motivate behaviours that facilitate energy acquisition, such as being bold or active in foraging. While there is evidence for links between metabolic rate and behaviour in constant environments, we know little about whether metabolic rate and behaviour change together when the environment changes-that is, if metabolic and behavioural plasticity co-vary. We investigated this using a fish that becomes dormant in winter and strongly reduces its activity when the environment cools, the cunner (Tautogolabrus adspersus). We found strong and predictable among-individual variation in thermal plasticity of metabolic rates, from resting to maximum levels, but no evidence for among-individual variation in thermal plasticity of movement activity, meaning that these key physiological and behavioural traits change independently when the environment changes. The strong among-individual variation in metabolic rate plasticity resulted in much higher repeatability (among-individual consistency) of metabolic rates at warm than cold temperatures, indicating that the potential for metabolic rate to evolve under selection is temperature-dependent, as repeatability can set the upper limit to heritability. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Thermal constraints on exercise and metabolic performance do not explain the use of dormancy as an overwintering strategy in the cunner (Tautogolabrus adspersus).

Winter cold slows ectotherm physiology, potentially constraining activities and ecological opportunities at poleward latitudes. Yet, many fishes are winter-active, facilitated by thermal compensation that improves cold performance. Conversely, winter-dormant fishes (e.g. cunner, Tautogolabrus adspersus) become inactive and non-feeding overwinter. Why are certain fishes winter-dormant? We hypothesized that winter dormancy is an adaptive behavioural response arising in poleward species that tolerate severe, uncompensated constraints of cold on their physiological performance. We predicted that below their dormancy threshold of 7--8°C, exercise and metabolic performance of cunner are greatly decreased, even after acclimation (i.e. shows above-normal, uncompensated thermal sensitivity, Q10>1-3). We measured multiple key performance metrics (e.g. C-start maximum velocity, chase swimming speed, aerobic scope) in cunner after acute exposure to 26-2°C (3°C intervals using 14°C-acclimated fish) or acclimation (5-8 weeks) to 14-2°C (3°C intervals bracketing the dormancy threshold). Performance declined with cooling, and the acute Q10 of all six performance rate metrics was significantly greater below the dormancy threshold temperature (Q10,acute8-2°C=1.5-4.9, mean=3.3) than above (Q10,acute14-8°C=1.1-1.9, mean=1.5), inferring a cold constraint. However, 2°C acclimation (temporally more relevant to seasonal cooling) improved performance, abolishing the acute constraint (Q10,acclimated8-2°C=1.4-3.0, mean=2.0; also cf. Q10,acclimated14-8°C=1.2-2.9, mean=1.7). Thus, dormant cunner show partial cold-compensation of exercise and metabolic performance, similar to winter-active species. However, responsiveness to C-start stimuli was greatly cold-constrained even following acclimation, suggesting dormancy involves sensory limitation. Thermal constraints on metabolic and exercise physiology are not significant drivers of winter dormancy in cunner. In fact, compensatory plasticity at frigid temperatures is retained even in a dormant fish.

Applied winter biology: threats, conservation and management of biological resources during winter in cold climate regions.

Winter at high latitudes is characterized by low temperatures, dampened light levels and short photoperiods which shape ecological and evolutionary outcomes from cells to populations to ecosystems. Advances in our understanding of winter biological processes (spanning physiology, behaviour and ecology) highlight that biodiversity threats (e.g. climate change driven shifts in reproductive windows) may interact with winter conditions, leading to greater ecological impacts. As such, conservation and management strategies that consider winter processes and their consequences on biological mechanisms may lead to greater resilience of high altitude and latitude ecosystems. Here, we use well-established threat and action taxonomies produced by the International Union of Conservation of Nature-Conservation Measures Partnership (IUCN-CMP) to synthesize current threats to biota that emerge during, or as the result of, winter processes then discuss targeted management approaches for winter-based conservation. We demonstrate the importance of considering winter when identifying threats to biodiversity and deciding on appropriate management strategies across species and ecosystems. We confirm our expectation that threats are prevalent during the winter and are especially important considering the physiologically challenging conditions that winter presents. Moreover, our findings emphasize that climate change and winter-related constraints on organisms will intersect with other stressors to potentially magnify threats and further complicate management. Though conservation and management practices are less commonly considered during the winter season, we identified several potential or already realized applications relevant to winter that could be beneficial. Many of the examples are quite recent, suggesting a potential turning point for applied winter biology. This growing body of literature is promising but we submit that more research is needed to identify and address threats to wintering biota for targeted and proactive conservation. We suggest that management decisions consider the importance of winter and incorporate winter specific strategies for holistic and mechanistic conservation and resource management.

Inactivity and the passive slowing effect of cold on resting metabolism as the primary drivers of energy savings in overwintering fishes.

Winter dormancy is a seasonal survival strategy common among temperate ectotherms, characterized by inactivity, fasting and low metabolic rates. Previous reports of metabolic rate depression (MRD) in winter-dormant ectotherms, including many fishes, may have resulted from confounding influences of temperature-dependent variation in activity on metabolic rate measurements. We hypothesize that, as demonstrated recently in the winter-dormant cunner (Tautogolabrus adspersus), inactivity and the passive physicochemical (Arrhenius) effect of cold on standard metabolic rate (SMR) are the common primary mechanisms underlying the low metabolic rates among winter-dormant fishes. Using automated video tracking, we investigated threshold temperatures for winter dormancy onset (major reductions in activity, increased sheltering and fasting) in four phylogenetically diverse teleost species reported to be winter dormant: cunner, pumpkinseed sunfish (Lepomis gibbosus), American eel (Anguilla rostrata) and mummichog (Fundulus heteroclitus). All species showed large activity and feeding reductions, but the magnitude of change and dormancy threshold temperature was species-specific. We propose that a continuum of overwintering responses exists among fishes from dormant to lethargic to active. The relationship between activity and metabolic rate was then measured using video-recorded automated respirometry during acute cooling and following cold acclimation in pumpkinseed, mummichog and eel. In all species, activity and metabolic rate were strongly correlated at all temperatures, and cooling caused reduced activity and metabolic rate. When variation in activity was controlled for across temperatures spanning the dormancy thresholds, the thermal sensitivity of metabolic rate including SMR indicated the predominance of passive physicochemical influences (mean Q10<3.5), rather than active MRD. Activity reductions and physicochemical slowing of metabolism owing to cold appear to be the primary energy-saving mechanisms in overwintering fishes.

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.