Despite plasticity, heatwaves are costly for a coral reef fish.

Climate change is intensifying extreme weather events, including marine heatwaves, which are prolonged periods of anomalously high sea surface temperature that pose a novel threat to aquatic animals. Tropical animals may be especially vulnerable to marine heatwaves because they are adapted to a narrow temperature range. If these animals cannot acclimate to marine heatwaves, the extreme heat could impair their behavior and fitness. Here, we investigated how marine heatwave conditions affected the performance and thermal tolerance of a tropical predatory fish, arceye hawkfish (Paracirrhites arcatus), across two seasons in Moorea, French Polynesia. We found that the fish's daily activities, including recovery from burst swimming and digestion, were more energetically costly in fish exposed to marine heatwave conditions across both seasons, while their aerobic capacity remained the same. Given their constrained energy budget, these rising costs associated with warming may impact how hawkfish prioritize activities. Additionally, hawkfish that were exposed to hotter temperatures exhibited cardiac plasticity by increasing their maximum heart rate but were still operating within a few degrees of their thermal limits. With more frequent and intense heatwaves, hawkfish, and other tropical fishes must rapidly acclimate, or they may suffer physiological consequences that alter their role in the ecosystem.

Coronary circulation enhances the aerobic performance of wild Pacific salmon.

Female Pacific salmon often experience higher mortality than males during their once-in-a-lifetime up-river spawning migration, particularly when exposed to secondary stressors (e.g. high temperatures). However, the underlying mechanisms remain unknown. One hypothesis is that female Pacific salmon hearts are more oxygen-limited than males and are less able to supply oxygen to the body's tissues during this demanding migration. Notably, female hearts have higher coronary blood flow, which could indicate a greater reliance on this oxygen source. Oxygen limitations can develop from naturally occurring coronary blockages (i.e., coronary arteriosclerosis) found in mature salmon hearts. If female hearts rely more heavily on coronary blood flow but experience similar arteriosclerosis levels as males, they will have disproportionately impaired aerobic performance. To test this hypothesis, we measured resting (RMR) and maximum metabolic rate (MMR), aerobic scope (AS) and acute upper thermal tolerance in coho salmon (Oncorhynchus kisutch) with an intact or artificially blocked coronary oxygen supply. We also assessed venous blood oxygen and chemistry (cortisol, ions, and metabolite concentrations) at different time intervals during recovery from exhaustive exercise. We found that coronary blockage impaired MMR, AS, and the partial pressure of oxygen in venous blood (PvO2) during exercise recovery but did not differ between sexes. Coronary ligation lowered acute upper thermal tolerance by 1.1°C. Though we did not find evidence of enhanced female reliance on coronary supply, our findings highlight the importance of coronary blood supply for mature wild salmon, where migration success may be linked to cardiac performance, particularly during warm water conditions.

Diet effects on ectotherm thermal performance.

The environment is changing rapidly, and considerable research is aimed at understanding the capacity of organisms to respond. Changes in environmental temperature are particularly concerning as most animals are ectothermic, with temperature considered a key factor governing their ecology, biogeography, behaviour and physiology. The ability of ectotherms to persist in an increasingly warm, variable, and unpredictable future will depend on their nutritional status. Nutritional resources (e.g. food availability, quality, options) vary across space and time and in response to environmental change, but animals also have the capacity to alter how much they eat and what they eat, which may help them improve their performance under climate change. In this review, we discuss the state of knowledge in the intersection between animal nutrition and temperature. We take a mechanistic approach to describe nutrients (i.e. broad macronutrients, specific lipids, and micronutrients) that may impact thermal performance and discuss what is currently known about their role in ectotherm thermal plasticity, thermoregulatory behaviour, diet preference, and thermal tolerance. We finish by describing how this topic can inform ectotherm biogeography, behaviour, and aquaculture research.

Genomic vulnerability of a freshwater salmonid under climate change.

Understanding the adaptive potential of populations and species is pivotal for minimizing the loss of biodiversity in this era of rapid climate change. Adaptive potential has been estimated in various ways, including based on levels of standing genetic variation, presence of potentially beneficial alleles, and/or the severity of environmental change. Kokanee salmon, the non-migratory ecotype of sockeye salmon (Oncorhynchus nerka), is culturally and economically important and has already been impacted by the effects of climate change. To assess its climate vulnerability moving forward, we integrated analyses of standing genetic variation, genotype-environment associations, and climate modeling based on sequence and structural genomic variation from 224 whole genomes sampled from 22 lakes in British Columbia and Yukon (Canada). We found that variables for extreme temperatures, particularly warmer temperatures, had the most pervasive signature of selection in the genome and were the strongest predictors of levels of standing variation and of putatively adaptive genomic variation, both sequence and structural. Genomic offset estimates, a measure of climate vulnerability, were significantly correlated with higher increases in extreme warm temperatures, further highlighting the risk of summer heat waves that are predicted to increase in frequency in the future. Levels of standing genetic variation, an important metric for population viability and resilience, were not correlated with genomic offset. Nonetheless, our combined approach highlights the importance of integrating different sources of information and genomic data to formulate more comprehensive and accurate predictions on the vulnerability of populations and species to future climate change.

Pairing lab and field studies to predict thermal performance of wild fish.

In thermally variable ecosystems, temperatures can change extensively on hourly and seasonal timescales requiring ectotherms to possess a broad thermal tolerance (critical thermal minima [CTmin] and maxima [CTmax]). However, whether fish acclimate in the laboratory similarly as they acclimatize in the field under comparable thermal variation is unclear. We used temperature data from a tidal salt marsh to design 21-day lab-acclimation treatments (static: 12, 17, 22, 27 °C; daily variation with mean 22 °C: i) range 17-27 °C, ii) range 17-27 °C with irregular extremes within 12-32 °C). We compared thermal limits in lab-acclimated and field-acclimatized eurythermal arrow goby (Clevelandia ios). Variable temperature-acclimated and acclimatized fish had similar CTmin and CTmax. Notably, arrow gobies showed rapid plasticity in their absolute thermal tolerance within one tidal cycle. The daily mean and max temperatures experienced were positively related to CTmax and CTmin, respectively. This study demonstrates that ecologically informed lab acclimation treatments can yield tolerance results that are applicable to wild fish.

Impairing cardiac oxygen supply in swimming coho salmon compromises their heart function and tolerance to acute warming.

Climatic warming elevates mortality for many salmonid populations during their physically challenging up-river spawning migrations, yet, the mechanisms underlying the increased mortality remain elusive. One hypothesis posits that a cardiac oxygen insufficiency impairs the heart's capacity to pump sufficient oxygen to body tissues to sustain up-river swimming, especially in warm water when oxygen availability declines and cardiac and whole-animal oxygen demand increases. We tested this hypothesis by measuring cardiac and metabolic (cardiorespiratory) performance, and assessing the upper thermal tolerance of coho salmon (Oncorhynchus kisutch) during sustained swimming and acute warming. By surgically ligating the coronary artery, which naturally accumulates arteriosclerotic lesions in migrating salmon, we partially impaired oxygen supply to the heart. Coronary ligation caused drastic cardiac impairment during swimming, even at benign temperatures, and substantially constrained cardiorespiratory performance during swimming and progressive warming compared to sham-operated control fish. Furthermore, upper thermal tolerance during swimming was markedly reduced (by 4.4 °C) following ligation. While the cardiorespiratory capacity of female salmon was generally lower at higher temperatures compared to males, upper thermal tolerance during swimming was similar between sexes within treatment groups. Cardiac oxygen supply is a crucial determinant for the migratory capacity of salmon facing climatic environmental warming.

Physiological differences between wild and captive animals: a century-old dilemma.

Laboratory-based research dominates the fields of comparative physiology and biomechanics. The power of lab work has long been recognized by experimental biologists. For example, in 1932, Georgy Gause published an influential paper in Journal of Experimental Biology describing a series of clever lab experiments that provided the first empirical test of competitive exclusion theory, laying the foundation for a field that remains active today. At the time, Gause wrestled with the dilemma of conducting experiments in the lab or the field, ultimately deciding that progress could be best achieved by taking advantage of the high level of control offered by lab experiments. However, physiological experiments often yield different, and even contradictory, results when conducted in lab versus field settings. This is especially concerning in the Anthropocene, as standard laboratory techniques are increasingly relied upon to predict how wild animals will respond to environmental disturbances to inform decisions in conservation and management. In this Commentary, we discuss several hypothesized mechanisms that could explain disparities between experimental biology in the lab and in the field. We propose strategies for understanding why these differences occur and how we can use these results to improve our understanding of the physiology of wild animals. Nearly a century beyond Gause's work, we still know remarkably little about what makes captive animals different from wild ones. Discovering these mechanisms should be an important goal for experimental biologists in the future.

Body size and temperature affect metabolic and cardiac thermal tolerance in fish.

Environmental warming is associated with reductions in ectotherm body sizes, suggesting that larger individuals may be more vulnerable to climate change. The mechanisms driving size-specific vulnerability to temperature are unknown but are required to finetune predictions of fisheries productivity and size-structure community responses to climate change. We explored the potential metabolic and cardiac mechanisms underlying these body size vulnerability trends in a eurythermal fish, barred surfperch. We acutely exposed surfperch across a large size range (5-700 g) to four ecologically relevant temperatures (16 °C, 12 °C, 20 °C, and 22 °C) and subsequently, measured their metabolic capacity (absolute and factorial aerobic scopes, maximum and resting metabolic rates; AAS, FAS, MMR, RMR). Additionally, we estimated the fish's cardiac thermal tolerance by measuring their maximum heart rates (fHmax) across acutely increasing temperatures. Barred surfperch had parallel hypoallometric scaling of MMR and RMR (exponent 0.81) and a weaker hypoallometric scaling of fHmax (exponent - 0.05) across all test temperatures. In contrast to our predictions, the fish's aerobic capacity was maintained across sizes and acute temperatures, and larger fish had greater cardiac thermal tolerance than smaller fish. These results demonstrate that thermal performance may be limited by different physiological constraints depending on the size of the animal and species of interest.

Mechanisms of cardiac collapse at high temperature in a marine teleost (Girella nigrians).

Heat-induced mortality in ectotherms may be attributed to impaired cardiac performance, specifically a collapse in maximum heart rate (fHmax), although the physiological mechanisms driving this phenomenon are still unknown. Here, we tested two proposed factors which may restrict cardiac upper thermal limits: noxious venous blood conditions and oxygen limitation. We hypothesized elevated blood [K+] (hyperkalemia) and low oxygen (hypoxia) would reduce cardiac upper thermal limits in a marine teleost (Girella nigricans), while high oxygen (hyperoxia) would increase thermal limits. We also hypothesized higher acclimation temperatures would exacerbate the harmful effects of an oxygen limitation. Using the Arrhenius breakpoint temperature test, we measured fHmax in acutely warmed fish under control (saline injected) and hyperkalemic conditions (elevated plasma [K+]) while exposed to hyperoxia (200% air saturation), normoxia (100% air saturation), or hypoxia (20% air saturation). We also measured ventricle lactate content and venous blood oxygen partial pressure (PO2) to determine if there were universal thresholds in either metric driving cardiac collapse. Elevated [K+] was not significantly correlated with any cardiac thermal tolerance metric. Hypoxia significantly reduced cardiac upper thermal limits (Arrhenius breakpoint temperature [TAB], peak fHmax, temperature of peak heart rate [TPeak], and temperature at arrhythmia [TARR]). Hyperoxia did not alter cardiac thermal limits compared to normoxia. There was no evidence of a species-wide threshold in ventricular [lactate] or venous PO2. Here, we demonstrate that oxygen limits cardiac thermal tolerance only in instances of hypoxia, but that other physiological processes are responsible for causing temperature-induced heart failure when oxygen is not limited.

Fish feces reveal diverse nutrient sources for coral reefs.

Consumers mediate nutrient cycling through excretion and egestion across most ecosystems. In nutrient-poor tropical waters such as coral reefs, nutrient cycling is critical for maintaining productivity. While the cycling of fish-derived inorganic nutrients via excretion has been extensively investigated, the role of egestion for nutrient cycling has remained poorly explored. We sampled the fecal contents of 570 individual fishes across 40 species, representing six dominant trophic guilds of coral reef fishes in Moorea, French Polynesia. We measured fecal macro- (proteins, carbohydrates, lipids) and micro- (calcium, copper, iron, magnesium, manganese, zinc) nutrients and compared the fecal nutrient quantity and quality across trophic guilds, taxa, and body size. Macro- and micronutrient concentrations in fish feces varied markedly across species. Genera and trophic guild best predicted fecal nutrient concentrations. In addition, nutrient composition in feces was unique among species within both trophic guilds (herbivores and corallivores) and genera (Acanthurus and Chaetodon). Particularly, certain coral reef fishes (e.g., Thalassoma hardwicke, Chromis xanthura, Chaetodon pelewensis and Acanthurus pyroferus) harbored relatively high concentrations of micronutrients (e.g., Mn, Mg, Zn and Fe, respectively) that are known to contribute to ocean productivity and positively impact coral physiological performances. Given the nutrient-rich profiles across reef fish feces, conserving holistic reef fish communities ensures the availability of nutritional pools on coral reefs. We therefore suggest that better integration of consumer egestion dynamics into food web models and ecosystem-scale processes will facilitate an improved understanding of coral reef functioning.

Population variability in thermal performance of pre-spawning adult Chinook salmon.

Climate change is causing large declines in many Pacific salmon populations. In particular, warm rivers are associated with high levels of premature mortality in migrating adults. The Fraser River watershed in British Columbia, Canada, supports some of the largest Chinook salmon (Oncorhynchus tshawytscha) runs in the world. However, the Fraser River is warming at a rate that threatens these populations at critical freshwater life stages. A growing body of literature suggests salmonids are locally adapted to their thermal migratory experience, and thus, population-specific thermal performance information can aid in management decisions. We compared the thermal performance of pre-spawning adult Chinook salmon from two populations, a coastal fall-run from the Chilliwack River (125 km cooler migration) and an interior summer-run from the Shuswap River (565 km warmer migration). We acutely exposed fish to temperatures reflecting current (12°C, 18°C) and future projected temperatures (21°C, 24°C) in the Fraser River and assessed survival, aerobic capacity (resting and maximum metabolic rates, absolute aerobic scope (AAS), muscle and ventricle citrate synthase), anaerobic capacity (muscle and ventricle lactate dehydrogenase) and recovery capacity (post-exercise metabolism, blood physiology, tissue lactate). Chilliwack Chinook salmon performed worse at high temperatures, indicated by elevated mortality, reduced breadth in AAS, enhanced plasma lactate and potassium levels and elevated tissue lactate concentrations compared with Shuswap Chinook salmon. At water temperatures exceeding the upper pejus temperatures (Tpejus, defined here as 80% of maximum AAS) of Chilliwack (18.7°C) and Shuswap (20.2°C) Chinook salmon populations, physiological performance will decline and affect migration and survival to spawn. Our results reveal population differences in pre-spawning Chinook salmon performance across scales of biological organization at ecologically relevant temperatures. Given the rapid warming of rivers, we show that it is critical to consider the intra-specific variation in thermal physiology to assist in the conservation and management of Pacific salmon.

Metabolic constraints and individual variation shape the trade-off between physiological recovery and anti-predator responses in adult sockeye salmon.

Metabolic scope represents the aerobic energy budget available to an organism to perform non-maintenance activities (e.g., escape a predator, recover from a fisheries interaction, compete for a mate). Conflicting energetic requirements can give rise to ecologically relevant metabolic trade-offs when energy budgeting is constrained. The objective of this study was to investigate how aerobic energy is utilized when individual sockeye salmon (Oncorhynchus nerka) are exposed to multiple acute stressors. To indirectly assess metabolic changes in free-swimming individuals, salmon were implanted with heart rate biologgers. The animals were then exercised to exhaustion or briefly handled as a control, and allowed to recover from this stressor for 48 h. During the first 2 h of the recovery period, individual salmon were exposed to 90 ml of conspecific alarm cues or water as a control. Heart rate was recorded throughout the recovery period. Recovery effort and time was higher in exercised fish, relative to control fish, whereas exposure to an alarm cue had no effect on either of these metrics. Individual routine heart rate was negatively correlated with recovery time and effort. Together, these findings suggest that metabolic energy allocation towards exercise recovery (i.e., an acute stressor; handling, chase, etc.) trumps anti-predator responses in salmon, although individual variation may mediate this effect at the population level.

The ecological relevance of critical thermal maxima methodology for fishes.

Critical thermal maxima methodology (CTM) has been used to infer acute upper thermal tolerance in fishes since the 1950s, yet its ecological relevance remains debated. In this study, the authors synthesize evidence to identify methodological concerns and common misconceptions that have limited the interpretation of critical thermal maximum (CTmax ; value for an individual fish during one trial) in ecological and evolutionary studies of fishes. They identified limitations of, and opportunities for, using CTmax as a metric in experiments, focusing on rates of thermal ramping, acclimation regimes, thermal safety margins, methodological endpoints, links to performance traits and repeatability. Care must be taken when interpreting CTM in ecological contexts, because the protocol was originally designed for ecotoxicological research with standardized methods to facilitate comparisons within study individuals, across species and contexts. CTM can, however, be used in ecological contexts to predict impacts of environmental warming, but only if parameters influencing thermal limits, such as acclimation temperature or rate of thermal ramping, are taken into account. Applications can include mitigating the effects of climate change, informing infrastructure planning or modelling species distribution, adaptation and/or performance in response to climate-related temperature change. The authors' synthesis points to several key directions for future research that will further aid the application and interpretation of CTM data in ecological contexts.

Diet changes thermal acclimation capacity, but not acclimation rate, in a marine ectotherm (Girella nigricans) during warming.

Global climate change is increasing thermal variability in coastal marine environments and the frequency, intensity and duration of marine heatwaves. At the same time, food availability and quality are being altered by anthropogenic environmental changes. Marine ectotherms often cope with changes in temperature through physiological acclimation, which can take several weeks and is a nutritionally demanding process. Here, we tested the hypothesis that different ecologically relevant diets (omnivorous, herbivorous, carnivorous) impact thermal acclimation rate and capacity, using a temperate omnivorous fish as a model (opaleye, Girella nigricans). We measured acute thermal performance curves for maximum heart rate because cardiac function has been observed to set upper thermal limits in ectotherms. Opaleye acclimated rapidly after raising water temperatures, but their thermal limits and acclimation rate were not affected by their diet. However, the fish's acclimation capacity for maximum heart rate was sensitive to diet, with fish in the herbivorous treatment displaying the smallest change in heart rate throughout acclimation. Mechanistically, ventricle fatty acid composition differed with diet treatment and was related to cardiac performance in ways consistent with homoviscous adaptation. Our results suggest that diet is an important, but often overlooked, determinant of thermal performance in ectotherms on environmentally relevant time scales.

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.

Copper toxicity does not affect low tide emersion tolerance of Mytilus galloprovincialis.

Intertidal mussels are well adapted to withstand emersion from water during low tide, but they may be intermittently exposed to waterborne toxicants such as copper, which targets physiological processes including metabolism, ammonia excretion, and osmoregulation. To determine if copper exposure damages intertidal organisms' ability to tolerate tidal emersion, Mediterranean mussels (Mytilus galloprovincialis) were exposed to copper for 96 h followed by 6 h of emersion. Oxygen uptake increased after copper exposure which suggests that copper accumulation caused moderate stress in the mussels, but ammonia excretion and anaerobic metabolism were unaffected by mixed copper and emersion exposures. Shell composition analyses indicate that cycles of copper exposure and tidal emersion may affect bivalve shell growth, but copper deposition into shells may decrease the metal's overall toxicity. Results suggest that copper does not damage M. galloprovincialis's tolerance to tidal emersion, and insight is provided into the mussel's ability to overcome mixed stressor exposures.

Differences in the behavior and diet between shoaling and solitary surgeonfish (Acanthurus triostegus).

Variation in behavior within marine and terrestrial species can influence the functioning of the ecosystems they inhabit. However, the contribution of social behavior to ecosystem function remains underexplored. Many coral reef fish species provide potentially insightful models for exploring how social behavior shapes ecological function because they exhibit radical intraspecific variation in sociality within a shared habitat. Here, we provide an empirical exploration on how the ecological function of a shoaling surgeonfish (Acanthurus triostegus) may differ from that of solitary conspecifics on two Pacific coral reefs combining insight from behavioral observations, stable isotope analysis, and macronutrient analysis of gut and fecal matter. We detected important differences in how the social mode of A. triostegus affected its spatial and feeding ecology, as well as that of other reef fish species. Specifically, we found increased distance traveled and area covered by shoaling fish relative to solitary A. triostegus. Additionally, shoaling A. triostegus primarily grazed within territories of other herbivorous fish and had piscivorous and nonpiscivorous heterospecific fish associated with the shoal, while solitary A. triostegus grazed largely grazed outside of any territories and did not have any such interactions with heterospecific fish. Results from stable isotope analysis show a difference in δ15N isotopes between shoaling and solitary fish, which suggests that these different social modes are persistent. Further, we found a strong interaction between social behavior and site and carbohydrate and protein percentages in the macronutrient analysis, indicating that these differences in sociality are associated with measurable differences in both the feeding ecology and nutrient excretion patterns. Our study suggests that the social behavior of individuals may play an important and underappreciated role in mediating their ecological function.

Intraspecific variability in thermal tolerance: a case study with coastal cutthroat trout.

Fish physiological performance is directly regulated by their thermal environment. Intraspecific comparisons are essential to ascertain the vulnerability of fish populations to climate change and to identify which populations may be more susceptible to extirpation and which may be more resilient to continued warming. In this study, we sought to evaluate how thermal performance varies in coastal cutthroat trout (Oncorhynchus clarki clarki) across four distinct watersheds in OR, USA. Specifically, we measured oxygen consumption rates in trout from the four watersheds with variable hydrologic and thermal regimes, comparing three ecologically relevant temperature treatments (ambient, annual maximum and novel warm). Coastal cutthroat trout displayed considerable intraspecific variability in physiological performance and thermal tolerance across the four watersheds. Thermal tolerance matched the historical experience: the coastal watersheds experiencing warmer ambient temperatures had higher critical thermal tolerance compared with the interior, cooler Willamette watersheds. Physiological performance varied across all four watersheds and there was evidence of a trade-off between high aerobic performance and broad thermal tolerance. Given the evidence of climate regime shifts across the globe, the uncertainty in both the rate and extent of warming and species responses in the near and long term, a more nuanced approach to the management and conservation of native fish species must be considered.

Effect of thermal variation on the cardiac thermal limits of a eurythermal marine teleost (Girella nigricans).

Although most animals live in complex, thermally variable environments, the impact of this variability on specific physiological systems is still unresolved. The ectotherm heart is known to change in both structure and function to ensure appropriate oxygen delivery under different thermal regimes, but the plasticity of the upper thermal limits of the heart under stable or variable thermal acclimation conditions remains unknown. To investigate the role of thermal variability on cardiac acclimation potential, we acclimated a eurythermal fish, opaleye (Girella nigricans), to three static temperature treatments (13, 16, and 19 °C) as well as two oscillating treatments which cycled between maximum and minimum temperatures every 12 h (13-19 °C and 16-22 °C). These temperatures and daily thermal ranges were chosen to mimic the conditions observed in the rocky intertidal environments in Santa Barbara, CA, USA where the fish were collected. We hypothesized that increasing temperature would increase upper thermal limits of the heart, and that variable acclimations would result in broader acute thermal performance curves (TPCs) compared to static acclimations. We measured maximum heart rate during acute warming to determine cardiac thermal performance (i.e., the temperature corresponding to the onset of cardiac arrythmia, the temperature at maximum heart rate, absolute maximum heart rate, and the Arrhenius breakpoint temperature) and construct acute TPCs. Rising static acclimation temperatures increased upper thermal limits but had no impact on peak maximum heart rate. The warmest static temperature did, however, cause a narrowing of the acute TPC. Fish acclimated to variable conditions had the same upper thermal limits compared to fish acclimated to static conditions with the same mean temperature in all metrics of thermal performance. Further, there was no significant broadening of the acute TPC. This study suggests that cardiac plasticity is robust to thermal variation in this eurythermal fish.