Pacific salmon in hot water: applying aerobic scope models and biotelemetry to predict the success of spawning migrations

Concern over global climate change is widespread, but quantifying relationships between temperature change and animal fitness has been a challenge for scientists. Our approach to this challenge was to study migratory Pacific salmon (Oncorhynchus spp.), fish whose lifetime fitness hinges on a once-in-a-lifetime river migration to natal spawning grounds. Here, we suggest that their thermal optimum for aerobic scope is adaptive for river migration at the population level. We base this suggestion on several lines of evidence. The theoretical line of evidence comes from a direct association between the temperature optimum for aerobic metabolic scope and the temperatures historically experienced by three Fraser River salmon populations during their river migration. This close association was then used to predict that the occurrence of a period of anomalously high river temperatures in 2004 led to a complete collapse of aerobic scope during river migration for a portion of one of the sockeye salmon (Oncorhynchus nerka) populations. This prediction was corroborated with empirical data from our biotelemetry studies, which tracked the migration of individual sockeye salmon in the Fraser River and revealed that the success of river migration for the same sockeye population was temperature dependent. Therefore, we suggest that collapse of aerobic scope was an important mechanism to explain the high salmon mortality observed during their migration. Consequently, models based on thermal optima for aerobic scope for ectothermic animals should improve predictions of population fitness under future climate scenarios.     

Modelling the future hydroclimatology of the lower Fraser River and its impacts on the spawning migration survival of sockeye salmon

Short episodic high temperature events can be lethal for migrating adult Pacific salmon (Oncorhynchus spp.). We downscaled temperatures for the Fraser River, British Columbia to evaluate the impact of climate warming on the frequency of exceeding thermal thresholds associated with salmon migratory success. Alarmingly, a modest 1.0 °C increase in average summer water temperature over 100 years (1981–2000 to 2081–2100) tripled the number of days per year exceeding critical salmonid thermal thresholds (i.e. 19.0 °C). Refined thresholds for two populations (Gates Creek and Weaver Creek) of sockeye salmon (Oncorhynchus nerka) were defined using physiological constraint models based on aerobic scope. While extreme temperatures leading to complete aerobic collapse remained unlikely under our warming scenario, both populations were increasingly forced to migrate upriver at reduced levels of aerobic performance (e.g. in 80% of future simulations, ≥90% of salmon encountered temperatures exceeding population‐specific thermal optima for maximum aerobic scope; T_opt=16.3 °C for Gates Creek and T_opt=14.5 °C for Weaver Creek). Assuming recent changes to river entry timing persist, we also predicted dramatic increases in the probability of freshwater mortality for Weaver Creek salmon due to reductions in aerobic, and general physiological, performance (e.g. in 42% of future simulations≥50% of Weaver Creek fish exceeded temperature thresholds associated with 0–60% of maximum aerobic scope). Potential for adaptation via directional selection on run‐timing was more evident for the Weaver Creek population. Early entry Weaver Creek fish experienced 25% (range: 15–31%) more suboptimal temperatures than late entrants, compared with an 8% difference (range: 0–17%) between early and late Gates Creek fish. Our results emphasize the need to consider daily temperature variability in association with population‐specific differences in behaviour and physiological constraints when forecasting impacts of climate change on migratory survival of aquatic species.     

Thermal acclimation is not necessary to maintain a wide thermal breadth of aerobic scope in the common killifish (Fundulus heteroclitus)

Loss of aerobic scope at high and low temperatures is a physiological mechanism proposed to limit the thermal performance and tolerance of organisms, a theory known as oxygen- and capacity-limited thermal tolerance (OCLTT). Eurythermal organisms maintain aerobic scope over wide ranges of temperatures, but it is unknown whether acclimation is necessary to maintain this breadth. The objective of this study was to examine changes in aerobic scope in Fundulus heteroclitus, a eurythermal fish, after acclimation and acute exposure to temperatures from 5° to 33°C. The range of temperatures over which aerobic scope was nonzero was similar in acclimated and acutely exposed fish, suggesting that acclimation has modest effects on the thermal breadth of aerobic scope. However, in acclimated fish, there was a clear optimum temperature range for aerobic scope between 25° and 30°C, whereas aerobic scope was relatively constant across the entire temperature range with acute temperature exposure. Therefore, the primary effect of acclimation was to increase aerobic scope between 25° and 30°C, which paradoxically resulted in a narrower temperature range of optimal performance in acclimated fish compared to acutely exposed fish. There was only weak evidence for correlations between the thermal optimum of aerobic scope and the thermal optimum of measures of performance (specific growth rate and gonadosomatic index), and indicators of anaerobic metabolism (lactate accumulation and lactate dehydrogenase activity) only increased at high temperatures. Together these data fit many, but not all, of the predictions made by OCLTT.     

The combined effect of body size and temperature on oxygen consumption rates and the size-dependency of preferred temperature in European perch Perca fluviatilis

The present study determined the effect of body mass and acclimation temperature (15–28°C) on oxygen consumption rate (ṀO₂) and the size dependency of preferred temperature in European perch Perca fluviatilis. Standard metabolic rate (SMR) scaled allometrically with body mass by an exponent of 0.86, and temperature influenced SMR with a Q₁₀ of 1.9 regardless of size. Maximum metabolic rate (MMR) and aerobic scope (MMR-SMR) scaled allometrically with body mass by exponents of 0.75–0.88. The mass scaling exponents of MMR and aerobic scope changed with temperature and were lowest at the highest temperature. Consequently, the optimal temperature for aerobic scope decreased with increasing body mass. Notably, fish <40 g did not show a decrease aerobic scope with increasing temperature. Factorial aerobic scope (MMR × SMR⁻¹) generally decreased with increasing temperatures, was unaffected by size at the lower temperatures, and scaled negatively with body mass at the highest temperature. Similar to the optimal temperature for aerobic scope, preferred temperature declined with increasing body mass, unaffectedly by acclimation temperature. The present study indicates a limitation in the capacity for oxygen uptake in larger fish at high temperatures. A constraint in oxygen uptake at high temperature may restrict the growth of larger fish with environmental warming, at least if food availability is not limited. Furthermore, behavioural thermoregulation may be contributing to regional changes in the size distribution of fish in the wild caused by global warming as larger individuals will prefer colder water at higher latitudes and at larger depths than smaller conspecifics with increasing environmental temperatures.     

Temperature,metabolic power and the evolution of endothermy

Endothermy has evolved at least twice, in the precursors to modern mammals and birds. The most widely accepted explanation for the evolution of endothermy has been selection for enhanced aerobic capacity. We review this hypothesis in the light of advances in our understanding of ATP generation by mitochondria and muscle performance. Together with the development of isotope‐based techniques for the measurement of metabolic rate in free‐ranging vertebrates these have confirmed the importance of aerobic scope in the evolution of endothermy: absolute aerobic scope, ATP generation by mitochondria and muscle power output are all strongly temperature‐dependent, indicating that there would have been significant improvement in whole‐organism locomotor ability with a warmer body. New data on mitochondrial ATP generation and proton leak suggest that the thermal physiology of mitochondria may differ between organisms of contrasting ecology and thermal flexibility. Together with recent biophysical modelling, this strengthens the long‐held view that endothermy originated in smaller, active eurythermal ectotherms living in a cool but variable thermal environment. We propose that rather than being a secondary consequence of the evolution of an enhanced aerobic scope, a warmer body was the means by which that enhanced aerobic scope was achieved. This modified hypothesis requires that the rise in metabolic rate and the insulation necessary to retain metabolic heat arose early in the lineages leading to birds and mammals. Large dinosaurs were warm, but were not endotherms, and the metabolic status of pterosaurs remains unresolved.     

Adapt,move or die – how will tropical coral reef fishes cope with ocean warming?

Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade, more than 365 tropical stenothermal fish species have been documented moving poleward, away from ocean warming hotspots where temperatures 2–3 °C above long‐term annual means can compromise critical physiological processes. We examined the capacity of a model species – a thermally sensitive coral reef fish, Chromis viridis (Pomacentridae) – to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least 6 weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end‐of‐century predicted temperatures (i.e. 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long‐term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating poleward migration of species.     

Potential for adaptation to climate change in a coral reef fish

Predicting the impacts of climate change requires knowledge of the potential to adapt to rising temperatures, which is unknown for most species. Adaptive potential may be especially important in tropical species that have narrow thermal ranges and live close to their thermal optimum. We used the animal model to estimate heritability, genotype by environment interactions and nongenetic maternal components of phenotypic variation in fitness‐related traits in the coral reef damselfish, Acanthochromis polyacanthus. Offspring of wild‐caught breeding pairs were reared for two generations at current‐day and two elevated temperature treatments (+1.5 and +3.0 °C) consistent with climate change projections. Length, weight, body condition and metabolic traits (resting and maximum metabolic rate and net aerobic scope) were measured at four stages of juvenile development. Additive genetic variation was low for length and weight at 0 and 15 days posthatching (dph), but increased significantly at 30 dph. By contrast, nongenetic maternal effects on length, weight and body condition were high at 0 and 15 dph and became weaker at 30 dph. Metabolic traits, including net aerobic scope, exhibited high heritability at 90 dph. Furthermore, significant genotype x environment interactions indicated potential for adaptation of maximum metabolic rate and net aerobic scope at higher temperatures. Net aerobic scope was negatively correlated with weight, indicating that any adaptation of metabolic traits at higher temperatures could be accompanied by a reduction in body size. Finally, estimated breeding values for metabolic traits in F2 offspring were significantly affected by the parental rearing environment. Breeding values at higher temperatures were highest for transgenerationally acclimated fish, suggesting a possible role for epigenetic mechanisms in adaptive responses of metabolic traits. These results indicate a high potential for adaptation of aerobic scope to higher temperatures, which could enable reef fish populations to maintain their performance as ocean temperatures rise.     

Little left in the tank: metabolic scaling in marine teleosts and its implications for aerobic scope

Fish larvae are the world's smallest vertebrates, and their high rates of mortality may be partially owing to a very limited aerobic scope. Unfortunately, however, no complete empirical dataset exists on the relationship between minimal and maximal metabolism (and thus aerobic scope) for any fish species throughout ontogeny, and thus such an association is hard to delineate. We measured standard and maximal metabolism in three marine fish species over their entire life history, and show that while aerobic scope depends greatly on body size and developmental trajectory, it is extremely small during the early life stages (factorial aerobic scope < or =1.5). Our findings strongly suggest that limited scope for aerobic activity early in life is likely to constrain physiological function and ultimately impact behaviour and possibly survival. Furthermore, our results have important implications for ecological models that incorporate metabolic scaling, and provide additional evidence against the existence of 'universal' scaling exponents.     

Life on the edge: thermal optima for aerobic scope of equatorial reef fishes are close to current day temperatures

Equatorial populations of marine species are predicted to be most impacted by global warming because they could be adapted to a narrow range of temperatures in their local environment. We investigated the thermal range at which aerobic metabolic performance is optimum in equatorial populations of coral reef fish in northern Papua New Guinea. Four species of damselfishes and two species of cardinal fishes were held for 14 days at 29, 31, 33, and 34 °C, which incorporated their existing thermal range (29–31 °C) as well as projected increases in ocean surface temperatures of up to 3 °C by the end of this century. Resting and maximum oxygen consumption rates were measured for each species at each temperature and used to calculate the thermal reaction norm of aerobic scope. Our results indicate that one of the six species, Chromis atripectoralis, is already living above its thermal optimum of 29 °C. The other five species appeared to be living close to their thermal optima (ca. 31 °C). Aerobic scope was significantly reduced in all species, and approached zero for two species at 3 °C above current‐day temperatures. One species was unable to survive even short‐term exposure to 34 °C. Our results indicate that low‐latitude reef fish populations are living close to their thermal optima and may be more sensitive to ocean warming than higher‐latitude populations. Even relatively small temperature increases (2–3 °C) could result in population declines and potentially redistribution of equatorial species to higher latitudes if adaptation cannot keep pace.     

Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity

Temperature imposes significant constraints on ectothermic animals, and these organisms have evolved numerous adaptations to respond to these constraints. While the impacts of temperature on the physiology of ectotherms have been extensively studied, there are currently no frameworks available that outline the multiple and often simultaneous pathways by which temperature can affect behaviour. Drawing from the literature on insects, we propose a unified framework that should apply to all ectothermic animals, generalizing temperature's behavioural effects into: (1) kinetic effects, resulting from temperature's bottom‐up constraining influence on metabolism and neurophysiology over a range of timescales (from short to long term), and (2) integrated effects, where the top‐down integration of thermal information intentionally initiates or modifies a behaviour (behavioural thermoregulation, thermal orientation, thermosensory behavioural adjustments). We discuss the difficulty in distinguishing adaptive behavioural changes from constraints when observing animals' behavioural responses to temperature. We then propose two complementary approaches to distinguish adaptations from constraints, and categorize behaviours according to our framework: (i) ‘kinetic null modelling’ of temperature's effects on behaviour; and (ii) behavioural ecology experiments using temperature‐insensitive mutants. Our framework should help to guide future research on the complex relationship between temperature and behaviour in ectothermic animals.     

Counter-Gradient Variation in Respiratory Performance of Coral Reef Fishes at Elevated Temperatures

The response of species to global warming depends on how different populations are affected by increasing temperature throughout the species'' geographic range. Local adaptation to thermal gradients could cause populations in different parts of the range to respond differently. In aquatic systems, keeping pace with increased oxygen demand is the key parameter affecting species'' response to higher temperatures. Therefore, respiratory performance is expected to vary between populations at different latitudes because they experience different thermal environments. We tested for geographical variation in respiratory performance of tropical marine fishes by comparing thermal effects on resting and maximum rates of oxygen uptake for six species of coral reef fish at two locations on the Great Barrier Reef (GBR), Australia. The two locations, Heron Island and Lizard Island, are separated by approximately 1200 km along a latitudinal gradient. We found strong counter-gradient variation in aerobic scope between locations in four species from two families (Pomacentridae and Apogonidae). High-latitude populations (Heron Island, southern GBR) performed significantly better than low-latitude populations (Lizard Island, northern GBR) at temperatures up to 5°C above average summer surface-water temperature. The other two species showed no difference in aerobic scope between locations. Latitudinal variation in aerobic scope was primarily driven by up to 80% higher maximum rates of oxygen uptake in the higher latitude populations. Our findings suggest that compensatory mechanisms in high-latitude populations enhance their performance at extreme temperatures, and consequently, that high-latitude populations of reef fishes will be less impacted by ocean warming than will low-latitude populations.     

Thermal growth potential of Atlantic cod by the end of the 21st century

Ocean warming may lead to smaller body sizes of marine ectotherms, because metabolic rates increase exponentially with temperature while the capacity of the cardiorespiratory system to match enhanced oxygen demands is limited. Here, we explore the impact of rising sea water temperatures on Atlantic cod (Gadus morhua), an economically important fish species. We focus on changes in the temperature‐dependent growth potential by a transfer function model combining growth observations with climate model ensemble temperatures. Growth potential is expressed in terms of asymptotic body weight and depends on water temperature. We consider changes between the periods 1985–2004 and 2081–2100, assuming that future sea water temperatures will evolve according to climate projections for IPCC AR5 scenario RCP8.5. Our model projects a response of Atlantic cod to future warming, differentiated according to ocean regions, leading to increases of asymptotic weight in the Barents Sea, while weights are projected to decline at the southern margin of the biogeographic range. Southern spawning areas will disappear due to thermal limitation of spawning stages. These projections match the currently observed biogeographic shifts and the temperature‐ and oxygen‐dependent decline in routine aerobic scope at southern distribution limits.     

Climate change in fish: effects of respiratory constraints on optimal life history and behaviour

The difference between maximum metabolic rate and standard metabolic rate is referred to as aerobic scope, and because it constrains performance it is suggested to constitute a key limiting process prescribing how fish may cope with or adapt to climate warming. We use an evolutionary bioenergetics model for Atlantic cod (Gadus morhua) to predict optimal life histories and behaviours at different temperatures. The model assumes common trade-offs and predicts that optimal temperatures for growth and fitness lie below that for aerobic scope; aerobic scope is thus a poor predictor of fitness at high temperatures. Initially, warming expands aerobic scope, allowing for faster growth and increased reproduction. Beyond the optimal temperature for fitness, increased metabolic requirements intensify foraging and reduce survival; oxygen budgeting conflicts thus constrain successful completion of the life cycle. The model illustrates how physiological adaptations are part of a suite of traits that have coevolved.     

Moult-related reduction of aerobic scope in passerine birds

It is well established that the nutrient and energy requirements of birds increase substantially during moult, but it is not known if these increased demands affect their aerobic capacity. We quantified the absolute aerobic scope of house and Spanish sparrows, Passer domesticus and P. hispaniolensis, respectively, before and during sequential stages of their moult period. The absolute aerobic scope (AAS) is the difference between maximum metabolic rate (MMR) during peak locomotor activities and minimum resting metabolic rate (RMR_min), thus representing the amount of aerobic power above that committed to maintenance needs available for other activities. As expected, RMR_min increased over the moult period by up to 40 and 63% in house and Spanish sparrows, respectively. Surprisingly, the maximum metabolic rates also decreased during moult in both species, declining as much as 25 and 38% compared with pre-moult values of house and Spanish sparrows, respectively. The concurrent changes in RMR_min and MMR during moult resulted in significant decreases in AAS, being up to 32 and 47% lower than pre-moult levels of house and Spanish sparrows, respectively, during moult stages having substantial feather replacement. We argue that the combination of reduced flight efficiency due to loss of wing feathers and reduced aerobic capacity places moulting birds at greater risk of predation. Such performance constraints likely contribute to most birds temporally separating moult from annual events requiring peak physiological capacity such as breeding and migration.

     

INVESTIGATING EVOLUTIONARY TRADE‐OFFS IN WILD POPULATIONS OF ATLANTIC SALMON (SALMO SALAR): INCORPORATING DETECTION PROBABILITIES AND INDIVIDUAL HETEROGENEITY

Evolutionary trade‐offs among demographic parameters are important determinants of life‐history evolution. Investigating such trade‐offs under natural conditions has been limited by inappropriate analytical methods that fail to address the bias in demographic estimates that can result when issues of detection (uncertain detection of individual) are ignored. We propose a new statistical approach to quantify evolutionary trade‐offs in wild populations. Our method is based on a state‐space modeling framework that focuses on both the demographic process of interest as well as the observation process. As a case study, we used individual mark–recapture data for stream‐dwelling Atlantic salmon juveniles in the Scorff River (Southern Brittany, France). In freshwater, juveniles face two life‐history choices: migration to the ocean and sexual maturation (for males). Trade‐offs may appear with these life‐history choices and survival, because all are energy dependent. We found a cost of reproduction on survival for fish staying in freshwater and a survival advantage associated with the “decision” to migrate. Our modeling framework opens up promising prospects for the study of evolutionary trade‐offs when some life‐history traits are not, or only partially, observable.     

Using maximum heart rate as a rapid screening tool to determine optimum temperature for aerobic scope in Pacific salmon Oncorhynchus spp

The mean ±s.e. optimum temperature (T(opt)) for aerobic scope in juvenile coho salmon Oncorhynchus kisutch was determined to be 17·0 ± 0·7° C. The repeated measures protocol took 3 weeks to complete the T(opt) determination using 12 fish tested at five temperatures separated by 2° C increments. This experiment also demonstrated that the T(opt) was associated with maximum heart rate (f(H)) failing to maintain a Q(10) -related increase with temperature. When maximum f(H) was produced in anaesthetized fish with pharmacological stimulation and f(H) measured from electrocardiogram recordings during acute warming, the Arrhenius break temperature (ABT) for Q(10) discontinuities in maximum f(H) (mean ±s.e. = 17·1 ± 0·5° C for 15 ppm clove oil and 16·5 ± 0·2° C for 50 ppm MS-222) was statistically indistinguishable from the T(opt) measured using aerobic scope. Such a determination took only 3 days rather than 3 weeks. Therefore, it is proposed that determining ABT for discontinuities in maximum f(H) in anaesthetized fish presents itself as a valuable, high-throughput screening tool to assess T(opt) in fishes, a metric that has become recognized as being extremely valuable in fish biology and fisheries management.     

五种淡水鱼类幼鱼游泳能力的比较

为了探讨栖息于不同生境中鱼类的游泳能力和偏好游泳速度及其生理机制,本研究以中华倒刺鲃(Spinibarbus sinensis)、异育银鲫(Carassius auratus gibelio)、岩原鲤(Procypris rabaudi)、青鱼(Mylopharyngodon piceus)和胭脂鱼(Myxocryprinus asiaticus)5种鱼的幼鱼为对象,在(25±1)℃条件下测定了5种鱼类的标准代谢率(SMR)、最大代谢率(MMR)、有氧代谢范围(MS)、临界游泳速度(Ucrit)、最大匀加速游泳速度(Ucat)和偏好游泳速度(Upref)。结果发现:5种实验鱼中,中华倒刺鲃的游泳能力最强,游泳能力较差的为青鱼和胭脂鱼;5种鱼之间的代谢和游泳能力差异显著,其偏好游泳速度主要集中在(10~24.5cm·s^-1)区域。研究表明,鱼类游泳能力的种间差异可能主要由心鳃系统相关的呼吸能力和体型相关的游泳效率所决定。本研究提供的有关鱼类游泳能力、偏好游泳速度等资料对于鱼道设计等有一定的参考价值。     

Warming temperatures and smaller body sizes: synchronous changes in growth of North Sea fishes

Decreasing body size has been proposed as a universal response to increasing temperatures. The physiology behind the response is well established for ectotherms inhabiting aquatic environments: as higher temperatures decrease the aerobic capacity, individuals with smaller body sizes have a reduced risk of oxygen deprivation. However, empirical evidence of this response at the scale of communities and ecosystems is lacking for marine fish species. Here, we show that over a 40‐year period six of eight commercial fish species in the North Sea examined underwent concomitant reductions in asymptotic body size with the synchronous component of the total variability coinciding with a 1–2 °C increase in water temperature. Smaller body sizes decreased the yield‐per‐recruit of these stocks by an average of 23%. Although it is not possible to ascribe these phenotypic changes unequivocally to temperature, four aspects support this interpretation: (i) the synchronous trend was detected across species varying in their life history and life style; (ii) the decrease coincided with the period of increasing temperature; (iii) the direction of the phenotypic change is consistent with physiological knowledge; and (iv) no cross‐species synchrony was detected in other species‐specific factors potentially impacting growth. Our findings support a recent model‐derived prediction that fish size will shrink in response to climate‐induced changes in temperature and oxygen. The smaller body sizes being projected for the future are already detectable in the North Sea.     

Can migrants escape from density dependence?

Migration is thought to maximize growth by enabling individuals to escape from density dependence, but this has rarely been tested at the individual level in natural populations. We employed linear mixed modeling of the spacing between consecutive scale growth rings to reconstruct individual growth profiles of a paradigmatic fish migrant, the sea trout (Salmo trutta) and related these to estimates of year class strength over a 13‐year period. Variation in scale growth was 1.3 times greater among individuals than within individuals in freshwater and 10 times greater at sea. Scale growth was inversely related to year class strength, both in freshwater (before migration) and at sea (after migration). Competition for patchily distributed resources is the most plausible explanation of the negative density‐dependent growth observed in freshwater and, to a lesser extent, in the marine environment. Our study provides some of the strongest evidence for a role of density dependence in determining partial migrations because although migrants can maximize growth by moving into the sea, they do not appear to become free from density dependence constraints completely. This has implications for conservation and suggests that sea trout and other anadromous fish displaying partial migrations may not be best managed on a river by river basis, but rather from a broader, coastal perspective.     

Disentangling environmental drivers of metabolic flexibility in birds: the importance of temperature extremes versus temperature variability

Examining physiological traits across large spatial scales can shed light on the environmental factors driving physiological variation. For endotherms, flexibility in aerobic metabolism is especially important for coping with thermally challenging environments and recent research has shown that aerobic metabolic scope [the difference between maximum thermogenic capacity (M_sum) and basal metabolic rate (BMR)] increases with latitude in mammals. One explanation for this pattern is the climatic variability hypothesis, which predicts that flexibility in aerobic metabolism should increase as a function of local temperature variability. An alternative explanation is the cold adaptation hypothesis, which predicts that cold temperature extremes may also be an important driver of variation in metabolic scope. To determine the thermal drivers of aerobic metabolic flexibility in birds, we combined data on metabolic scope from 40 bird species sampled across a range of environments with several indices of local ambient temperature. Using phylogenetically‐informed analyses, we found that minimum winter temperature was the best predictor of variation in avian metabolic scope, outperforming all other thermal variables. Additionally, M_sum was a better predictor of latitudinal patterns of metabolic scope than BMR, with species inhabiting colder environments exhibiting increased M_sum over their counterparts in warmer environments. Taken together, these results suggest that cold temperature extremes drive latitudinal patterns of metabolic scope via selection for enhanced thermogenic performance in cold environments, supporting the cold adaptation hypothesis. Temperature extremes may therefore be an important selective pressure driving macrophysiological trends of aerobic performance in endotherms.