Alexander G. Little

Phenotypic plasticity can represent a vital adaptive response to environmental stressors, including those associated with climate change. Despite its evolutionary advantages, the expression of plasticity varies significantly within and among species, and is likely to be influenced by local environmental conditions. This variability in plasticity has important implications for evolutionary biology and conservation physiology. Theoretical models suggest that plasticity might incur intrinsic fitness costs, although the empirical evidence is inconsistent and there is ambiguity in the term ‘cost of plasticity’. Here, we systematically review the literature to investigate the prevalence of costs associated with phenotypic plasticity in ectothermic animals. We categorized studies into those assessing ‘costs of phenotype’ (trade-offs between different plastic trait values) and ‘costs of plasticity’ (intrinsic costs of the capacity for plasticity). Importantly, the experimental designs required to detect costs of plasticity are inherently more complex and onerous than those required to detect costs of phenotype. Accordingly, our findings reveal a significant focus on costs of phenotype over costs of plasticity, with the former more frequently detecting costs. Contrary to theoretical expectations, our analysis suggests that costs of plasticity are neither universal nor widespread. This raises questions about the evolutionary dynamics of plasticity, particularly in stable environments. Our analysis underscores the need for precise terminology and methodology in researching costs of plasticity, to avoid conflating costs associated with plastic traits with costs more intrinsic to plasticity. Understanding these nuances is crucial for predicting how species might adapt to rapidly changing environments.

Female-biased mortality has been consistently reported in Pacific salmon during their adult upriver migration. We collected coho salmon ( Oncorhynchus kisutch (Walbaum, 1792)) upon arrival at their spawning grounds to test whether females are more prone to cardiac oxygen limitations following exercise stress. We used a surgical approach to periodically sample arterial and venous blood over 48 h following recovery from a chase protocol to induce maximum metabolic rate. We found no significant differences in arterial or venous partial pressures of O₂ between males and females. Female salmon had significantly elevated plasma cortisol levels but there were no effects of sex on either plasma lactate or K⁺. Our data show that female coho salmon do not suffer oxygen limitations to the spongy myocardium after a single exercise event at moderate temperatures (14 °C)—at least not when arriving to their spawning grounds. This study found no clear support for a cardiac oxygen limitation underlying elevated female mortality in Pacific salmon. Neither, however, does our study design nor specific findings allow us to rule out cardiac limitations in these fish. Future work should address whether potential oxygen limitations to the spongy myocardium at high temperatures or oxygen limitations to the compact myocardium via coronary blood flow contribute to female-biased mortality earlier on the migratory route.

This review serves as an introduction to a special issue of Frontiers in Physiology, focused on the importance of physiological performance curves across phylogenetic and functional boundaries. Biologists have used performance curves to describe the effects of changing environmental conditions on animal physiology since the late 1800s (at least). Animal physiologists have studied performance curves extensively over the past decades, and there is a good foundation to understanding how the environment affects physiological functions of individuals. Our goal here was to build upon this research and address outstanding questions regarding the mutability and applicability of performance curves across taxonomic groups and levels of biological organization. Performance curves are not fixed at a taxonomic, population, or individual level – rather they are dynamic and can shift in response to evolutionary pressures (e.g., selection) and epigenetic programming (e.g., plasticity). The mechanisms underlying these shifts are being increasingly used to predict the efficacy with which plasticity and heritability of performance curves can render individuals and populations less vulnerable to climate change. Individual differences in physiological performance curves (and plasticity of performance curves) can also have cascading effects at higher levels of biological organization. For instance, individual physiology likely influences group behaviors in non-additive ways. There is a need therefore to extend the concept of performance curves to social interactions and sociality. Collectively, this special issue emphasizes the power of how within- and between-individual shifts in performance curves might scale up to the population-, species-, and community-level dynamics that inform conservation management strategies.

Intra-group social stability is important for the long-term productivity and health of social organisms. We evaluated the effect of group size on group stability in the face of repeated social perturbations using a cooperatively breeding fish, Neolamprologus pulcher. In a laboratory study, we compared both the social and physiological responses of individuals from small versus large groups to the repeated removal and replacement of the most dominant group member (the breeder male), either with a new male (treatment condition) or with the same male (control condition). Individuals living in large groups were overall more resistant to instability but were seemingly slower to recover from perturbation. Members of small groups were more vulnerable to instability but recovered faster. Breeder females in smaller groups also showed greater physiological preparedness for instability following social perturbations. In sum, we discover both behavioral and physiological evidence that living in larger groups helps to dampen the impacts of social instability in this system.

Environmental signals act primarily on physiological systems, which then influence higher‐level functions such as movement patterns and population dynamics. Increases in average temperature and temperature variability associated with global climate change are likely to have strong effects on fish physiology and thereby on populations and fisheries. Here we review the principal mechanisms that transduce temperature signals and the physiological responses to those signals in fish. Temperature has a direct, thermodynamic effect on biochemical reaction rates. Nonetheless, plastic responses to longer‐term thermal signals mean that fishes can modulate their acute thermal responses to compensate at least partially for thermodynamic effects. Energetics are particularly relevant for growth and movement, and therefore for fisheries, and temperature can have pronounced effects on energy metabolism. All energy (ATP) production is ultimately linked to mitochondria, and temperature has pronounced effects on mitochondrial efficiency and maximal capacities. Mitochondria are dependent on oxygen as the ultimate electron acceptor so that cardiovascular function and oxygen delivery link environmental inputs with energy metabolism. Growth efficiency, that is the conversion of food into tissue, changes with temperature, and there are indications that warmer water leads to decreased conversion efficiencies. Moreover, movement and migration of fish relies on muscle function, which is partially dependent on ATP production but also on intracellular calcium cycling within the myocyte. Neuroendocrine processes link environmental signals to regulated responses at the level of different tissues, including muscle. These physiological processes within individuals can scale up to population responses to climate change. A mechanistic understanding of thermal responses is essential to predict the vulnerability of species and populations to climate change.

Both laboratory and field respirometry are rapidly growing techniques to determine animal performance thresholds. However, replicating protocols to estimate maximum metabolic rate (MMR) between species, populations, and individuals can be difficult, especially in the field. We therefore evaluated seven different exercise treatments-four laboratory methods involving a swim tunnel (critical swim speed [Ucrit], Ucrit postswim fatigue, maximum swim speed [Umax], and Umax postswim fatigue) and three field-based chasing methods (3-min chase with 1-min air exposure, 3-min chase with no air exposure, and chase to exhaustion)-in adult coho salmon (Oncorhynchus kisutch) as a case study to determine best general practices for measuring and quantifying MMR in fish. We found that all seven methods were highly comparable and that chase treatments represent a valuable field alternative to swim tunnels. Moreover, we caution that the type of test and duration of measurement windows used to calculate MMR can have significant effects on estimates of MMR and statistical power for each approach.

Female-biased mortality has been repeatedly reported in Pacific salmon during their upriver migration in both field studies and laboratory-holding experiments, especially in the presence of multiple environmental stressors, including thermal stress. Here we used coho salmon (Oncorhynchus kisutch) to test whether females exposed to elevated water temperatures (18°C) i) suppress circulating sex hormones (testosterone, 11-ketotestosterone, and estradiol), owing to elevated cortisol levels, ii) have higher activities of enzymes supporting anaerobic metabolism (e.g., lactate dehydrogenase), iii) lower activities of enzymes driving oxidative metabolism (e.g., citrate synthase; CS), in skeletal and cardiac muscle, and iv) have more oxidative stress damage and reduced capacity for antioxidant defense (lower catalase activity; CAT). We found no evidence that a higher susceptibility to oxidative stress contributes to female-biased mortality at warm temperatures. We did, however, find that females had significantly lower cardiac LDH and that 18°C significantly reduced plasma levels of testosterone and estradiol, especially in females. We also found that relative gonad size was significantly lower in the 18°C treatment regardless of sex, whereas relative liver size was significantly lower in females held at 18°C. Further, relative spleen size was significantly elevated in the 18°C treatments across both sexes, with larger warm-induced increases in females. Our results suggest that males may better tolerate bouts of cardiac hypoxia at high temperature, and that thermal stress may also disrupt testosterone- and estradiol-mediated protein catabolism, and the immune response (larger spleens) in migratory female salmon.