The combined effects of reactant kinetics and enzyme stability explain the temperature dependence of metabolic rates

A mechanistic understanding of the response of metabolic rate to temperature is essential for understanding thermal ecology and metabolic adaptation. Although the Arrhenius equation has been used to describe the effects of temperature on reaction rates and metabolic traits, it does not adequately describe two aspects of the thermal performance curve (TPC) for metabolic rate—that metabolic rate is a unimodal function of temperature often with maximal values in the biologically relevant temperature range and that activation energies are temperature dependent. We show that the temperature dependence of metabolic rate in ectotherms is well described by an enzyme‐assisted Arrhenius (EAAR) model that accounts for the temperature‐dependent contribution of enzymes to decreasing the activation energy required for reactions to occur. The model is mechanistically derived using the thermodynamic rules that govern protein stability. We contrast our model with other unimodal functions that also can be used to describe the temperature dependence of metabolic rate to show how the EAAR model provides an important advance over previous work. We fit the EAAR model to metabolic rate data for a variety of taxa to demonstrate the model's utility in describing metabolic rate TPCs while revealing significant differences in thermodynamic properties across species and acclimation temperatures. Our model advances our ability to understand the metabolic and ecological consequences of increases in the mean and variance of temperature associated with global climate change. In addition, the model suggests avenues by which organisms can acclimate and adapt to changing thermal environments. Furthermore, the parameters in the EAAR model generate links between organismal level performance and underlying molecular processes that can be tested for in future work.     

鼎突多刺蚁热适应及运动行为的热依赖性

将鼎突多刺蚁(Polyrhachis vicina)分别置于15、20、25和30℃的恒温恒湿培养箱内,对其热适应及运动行为的热依赖性进行了研究。驯化2周后,采用温度梯度仪测量其热适应参数,并选用停顿频率(PF)、疾跑速度(SS)和最大持续运动距离(MDCCL)来衡量其运动能力。结果表明,驯化温度对鼎突多刺蚁的热适应和运动行为有极显著影响(P<0.01)。最适温度(PT)、临界低温(CLT)、临界高温(CHT)随驯化温度(AT)的升高而增大,最终适温为30.54℃,临界低温不低于3℃,临界高温不高于45℃;经过高温驯化的鼎突多刺蚁的运动能力显著大于经过低温驯化的个体运动能力,驯化温度与疾跑速度、最大持续运动距离呈显著的正相关,而与停顿频率呈极显著的负相关。     

热驯化对鼎突多刺蚁热适应和运动行为的影响

为比较恒温和变温驯化对鼎突多刺蚁（Polyrhachis vicina Roger）热适应和运动行为的影响,将鼎突多翅蚁分别在15℃恒温和13.4～21.6℃变温下进行驯化,定量分析两种驯化温度对鼎突多翅蚁热适应和运动行为的影响.结果表明,恒温和变温驯化对鼎突多刺蚁的最适温度、逃避高温、运动中的停顿频率、疾跑速度、最大持续运动距离均有显著影响（p＜0.01）,而对逃避低温的影响不显著（p=0.343）;变温驯化后鼎突多刺蚁的最适温度仅有一个峰值,这不符合最适性模型的预测;恒温和变温驯化下鼎突多刺蚁的疾跑速度与最大持续运动距离都呈显著的正相关（分别为p=0.017和p＜0.001）,且经过变温驯化的鼎突多刺蚁的运动能力明显强于恒温驯化下个体的运动能力.     

Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures?

Thermal performance curves (TPCs), which quantify how an ectotherm's body temperature (T_b) affects its performance or fitness, are often used in an attempt to predict organismal responses to climate change. Here, we examine the key – but often biologically unreasonable – assumptions underlying this approach; for example, that physiology and thermal regimes are invariant over ontogeny, space and time, and also that TPCs are independent of previously experienced T_b. We show how a critical consideration of these assumptions can lead to biologically useful hypotheses and experimental designs. For example, rather than assuming that TPCs are fixed during ontogeny, one can measure TPCs for each major life stage and incorporate these into stage‐specific ecological models to reveal the life stage most likely to be vulnerable to climate change. Our overall goal is to explicitly examine the assumptions underlying the integration of TPCs with T_b, to develop a framework within which empiricists can place their work within these limitations, and to facilitate the application of thermal physiology to understanding the biological implications of climate change.     

High predictability of direct competition between marine diatoms under different temperatures and nutrient states

The distribution of marine phytoplankton will shift alongside changes in marine environments, leading to altered species frequencies and community composition. An understanding of the response of mixed populations to abiotic changes is required to adequately predict how environmental change may affect the future composition of phytoplankton communities. This study investigated the growth and competitive ability of two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana, along a temperature gradient (9–35°C) spanning the thermal niches of both species under both high‐nitrogen nutrient‐replete and low‐nitrogen nutrient‐limited conditions. Across this temperature gradient, the competitive outcome under both nutrient conditions at any assay temperature, and the critical temperature at which competitive advantage shifted from one species to the other, was well predicted by the temperature dependencies of the growth rates of the two species measured in monocultures. The temperature at which the competitive advantage switched from P. tricornutum to T. pseudonana increased from 18.8°C under replete conditions to 25.3°C under nutrient‐limited conditions. Thus, P. tricornutum was a better competitor over a wider temperature range in a low N environment. Being able to determine the competitive outcomes from physiological responses of single species to environmental changes has the potential to significantly improve the predictive power of phytoplankton spatial distribution and community composition models.     

Individual variation in thermal plasticity and its impact on mass-scaling

Physiological processes vary widely across individuals and can influence how individuals respond to environmental change. Repeatability in how metabolic rate changes across temperatures (i.e. metabolic thermal plasticity) can influence mass-scaling exponents in different thermal environments. Moreover, repeatable plastic responses are necessary for reaction norms to respond to selective forces which is important for populations living in fluctuating environments. Nonetheless, only a small number of studies have explicitly quantified repeatability in metabolic plasticity, and fewer have explored how it can impact mass-scaling. We repeatedly measured standard metabolic rate of n = 42 delicate skinks Lampropholis delicata at six temperatures over the course of four months (N_{[observations]} = 4952). Using hierarchical statistical techniques, we accounted for multi-level variation and measurement error in our data in order to obtain more precise estimates of reaction norm repeatability and mass-scaling exponents at different acute temperatures. Our results show that individual differences in metabolic thermal plasticity were somewhat consistent over time (R_slope = 0.25, 95% CI = 2.48 × 10⁻⁸ – 0.67), however estimates were associated with a large degree of error. After accounting for measurement error, which decreased steadily with temperature, we show that among individual variance remained consistent across all temperatures. Congruently, temperature specific repeatability of average metabolic rate was stable across temperatures. Cross-temperature correlations were positive but were not uniform across the reaction norm. After taking into account multiple sources of variation, our estimates for mass-scaling did not change with temperature and were in line with published values for snakes and lizards. This implies that repeatable plastic responses may promote thermal stability of scaling exponents. Our work contributes to understanding how energy expenditure scales with abiotic and biotic factors and the capacity for reaction norms to respond to selection.     

The complex drivers of thermal acclimation and breadth in ectotherms

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid‐latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.     

The evolutionary potential of an insect invader under climate change*

Although the impacts of climate change and invasive species are typically studied in isolation, they likely interact to reduce the viability of plant and animal populations. Indeed, invasive species, by definition, have succeeded in areas outside of their native range and may therefore have higher adaptive capacity relative to native species. Nevertheless, the genetic architecture of the thermal niche, which sets a limit to the potential for populations to evolve rapidly under climate change, has never been measured in an invasive species in its introduced range. Here, we estimate the genetic architecture of thermal performance in the harlequin beetle (Harmonia axyridis), a Central Asian species that has invaded four continents. We measured thermal performance curves in more than 400 third-generation offspring from a paternal half-sib breeding experiment and analyzed the genetic variance–covariance matrix. We show that while the critical thermal limits in this species have an additive genetic basis, most components of the thermal performance curve have low heritability. Moreover, we found evidence that genetic correlations may constrain the evolution of beetles under climate change. Our results suggest that some invasive species may have limited evolutionary capacity under climate change, despite their initial success in colonizing novel environments.     

A resurrection study reveals limited evolution of thermal performance in response to recent climate change across the geographic range of the scarlet monkeyflower

Evolutionary rescue can prevent populations from declining under climate change, and should be more likely at high-latitude, “leading” edges of species’ ranges due to greater temperature anomalies and gene flow from warm-adapted populations. Using a resurrection study with seeds collected before and after a 7-year period of record warming, we tested for thermal adaptation in the scarlet monkeyflower Mimulus cardinalis. We grew ancestors and descendants from northern-edge, central, and southern-edge populations across eight temperatures. Despite recent climate anomalies, populations showed limited evolution of thermal performance curves. However, one southern population evolved a narrower thermal performance breadth by 1.31°C, which matches the direction and magnitude of the average decrease in seasonality experienced. Consistent with the climate variability hypothesis, thermal performance breadth increased with temperature seasonality across the species’ geographic range. Inconsistent with performance trade-offs between low and high temperatures across populations, we did not detect a positive relationship between thermal optimum and mean temperature. These findings fail to support the hypothesis that evolutionary response to climate change is greatest at the leading edge, and suggest that the evolution of thermal performance is unlikely to rescue most populations from the detrimental effects of rapidly changing climate.     

Thermal acclimation of swimming performance in newt larvae: the influence of diel temperature fluctuations during embryogenesis

1.  Thermal acclimation is one of the basic strategies by which organisms cope with thermal heterogeneity of the environment. Under predictable variation in environmental temperatures, theory predicts that selection favours acclimation of thermal performance curves over fixed phenotypes.
2.  We examined the influence of diel fluctuations in developmental temperatures on the thermal sensitivity of the maximal swimming capacity in larvae of the alpine newt, Triturus alpestris .
3.  We incubated newt eggs under three thermal regimes with varying daily amplitudes (1, 5 and 9 °C) and similar means (17·6–17·9 °C), and accordingly we measured the swimming speed of hatched larvae at three experimental temperatures (12, 17 and 22 °C), which they would normally experience in their natural habitat.
4.  Embryonic development under low and middle temperature fluctuations produced larvae with similar swimming speeds across experimental temperatures. In contrast, the most fluctuating regime induced development of phenotypes, which at 12 °C swam faster than larvae developed under moderate diel fluctuations.
5.  Our results provide evidence that diel temperature fluctuations induce acclimation of thermal dependence of locomotor performance. In ectotherms experiencing diel cycles in environmental temperatures, this plastic response may act as an important pacemaker in the evolution of thermal sensitivity.     

Differences in the thermal physiology of adult Yarrow's spiny lizards (Sceloporus jarrovii) in relation to sex and body size

Sexual size dimorphism (SSD) is often assumed to reflect the phenotypic consequences of differential selection operating on each sex. Species that exhibit SSD may also show intersexual differences in other traits, including field‐active body temperatures, preferred temperatures, and locomotor performance. For these traits, differences may be correlated with differences in body size or reflect sex‐specific trait optima. Male and female Yarrow's spiny lizards, Sceloporus jarrovii, in a population in southeastern Arizona exhibit a difference in body temperature that is unrelated to variation in body size. The observed sexual variation in body temperature may reflect divergence in thermal physiology between the sexes. To test this hypothesis, we measured the preferred body temperatures of male and female lizards when recently fed and fasted. We also estimated the thermal sensitivity of stamina at seven body temperatures. Variation in these traits provided an opportunity to determine whether body size or sex‐specific variation unrelated to size shaped their thermal physiology. Female lizards, but not males, preferred a lower body temperature when fasted, and this pattern was unrelated to body size. Larger individuals exhibited greater stamina, but we detected no significant effect of sex on the shape or height of the thermal performance curves. The thermal preference of males and females in a thermal gradient exceeded the optimal temperature for performance in both sexes. Our findings suggest that differences in thermal physiology are both sex‐ and size‐based and that peak performance at low body temperatures may be adaptive given the reproductive cycles of this viviparous species. We consider the implications of our findings for the persistence of S. jarrovii and other montane ectotherms in the face of climate warming.     

Intraspecific variation in tolerance of warming in fishes

Intraspecific variation in key traits such as tolerance of warming can have profound effects on ecological and evolutionary processes, notably responses to climate change. The empirical evidence for three primary elements of intraspecific variation in tolerance of warming in fishes is reviewed. The first is purely mechanistic that tolerance varies across life stages and as fishes become mature. The limited evidence indicates strongly that this is the case, possibly because of universal physiological principles. The second is intraspecific variation that is because of phenotypic plasticity, also a mechanistic phenomenon that buffers individuals’ sensitivity to negative impacts of global warming in their lifetime, or to some extent through epigenetic effects over successive generations. Although the evidence for plasticity in tolerance to warming is extensive, more work is required to understand underlying mechanisms and to reveal whether there are general patterns. The third element is intraspecific variation based on heritable genetic differences in tolerance, which underlies local adaptation and may define long-term adaptability of a species in the face of ongoing global change. There is clear evidence of local adaptation and some evidence of heritability of tolerance to warming, but the knowledge base is limited with detailed information for only a few model or emblematic species. There is also strong evidence of structured variation in tolerance of warming within species, which may have ecological and evolutionary significance irrespective of whether it reflects plasticity or adaptation. Although the overwhelming consensus is that having broader intraspecific variation in tolerance should reduce species vulnerability to impacts of global warming, there are no sufficient data on fishes to provide insights into particular mechanisms by which this may occur.     

Predicting the growth of the amphibian chytrid fungus in varying temperature environments

Environmental temperature is a crucial abiotic factor that influences the success of ectothermic organisms, including hosts and pathogens in disease systems. One example is the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd), which has led to widespread amphibian population declines. Understanding its thermal ecology is essential to effectively predict outbreaks. Studies that examine the impact of temperature on hosts and pathogens often do so in controlled constant temperatures. Although varying temperature experiments are becoming increasingly common, it is unrealistic to test every temperature scenario. Thus, reliable methods that use constant temperature data to predict performance in varying temperatures are needed. In this study, we tested whether we could accurately predict Bd growth in three varying temperature regimes, using a Bayesian hierarchical model fit with constant temperature Bd growth data. We fit the Bayesian hierarchical model five times, each time changing the thermal performance curve (TPC) used to constrain the logistic growth rate to determine how TPCs influence the predictions. We then validated the model predictions using Bd growth data collected from the three tested varying temperature regimes. Although all TPCs overpredicted Bd growth in the varying temperature regimes, some functional forms performed better than others. Varying temperature impacts on disease systems are still not well understood and improving our understanding and methodologies to predict these effects could provide insights into disease systems and help conservation efforts.     

Acclimation is beneficial at extreme test temperatures in the Danube crested newt, Triturus dobrogicus (Caudata, Salamandridae)

Despite many studies demonstrating the effect of acclimation on behavioural or physiological traits, considerable debate still exists about the evolutionary significance of this phenomenon. One of the unresolved issues is whether acclimation to warmer temperature is beneficial at treatment or at more extreme test temperatures. To answer this question, we assessed the effect of thermal acclimation on preferred body temperatures ( T _ps), maximum swimming and running speed, and critical thermal maximum ( CT _max) in the Danube crested newt ( Triturus dobrogicus ). Adult newts were kept at 15 °C (control) and 25 °C (treatment) for 8 weeks prior to measurements. We measured T _ps in an aquatic thermal gradient over 24 h, maximum speeds in a linear racetrack at six temperatures (5–33 °C), and CT _max in a continuously heated water bath. T _ps were higher in newts kept at 15 °C than in those kept at 25 °C. The maximum swimming speed did not acclimate. The maximum running speed at 30–33 °C was substantially higher in newts kept at 25 °C than in those kept at 15 °C. CT _max increased with the treatment temperature. Hence, we conclude that the acclimation response to warm temperature is beneficial not at treatment but at more extreme temperatures in newts.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 627–636.     

Sex cells in changing environments: can organisms adjust the physiological function of gametes to different temperatures?

Over the past decade, hundreds of studies have examined the abilities of whole organisms to modify their physiology and behaviour in response to environmental temperature changes; despite this, virtually nothing is known about the ability of sex cells to adjust to different temperature conditions. In fact, a recent meta‐analysis based on studies of 309 species and 112 physiological and ecological traits found no studies examining the influence of temperature on gamete function. Because sex cells play a critical role in the adaptation and persistence of species, this represents a severe oversight in physiological studies of thermal adaptation. Our study examines whether sex cells can respond phenotypically to variation in the thermal environment that is experienced by the whole‐organism. Specifically, we studied the thermal dependence of sperm swimming and the critical thermal limits of sperm cells in males of the poeciliid fish, Gambusia holbrooki. This species is well known for its ability to modify physiological function and maintains burst and sustained swimming performance and mating ability across a wide range of thermal conditions. In contrast, we found that sperm cells from male G. holbrooki did not adjust their physiological function as predicted by adaptive models. After acclimation of adult males to cool or warm temperatures, we found that the critical thermal limits of sperm function remained unchanged, as did the effect of temperature on sperm swimming performance. However, warm‐acclimated fish had sperm with higher swimming speeds across all temperatures. The absence of phenotypic changes in the critical thermal limits of sperm or thermal dependence of sperm swimming performance is surprising given that whole‐organism traits in G. holbrooki generally show improved performance after exposure to novel environments. As such an inability to thermally adjust gamete function may be widespread among other organisms, we urge biologists to investigate the generality of this result.     

Growth,developmental and stress responses of larvae of the clouded sulphur butterfly Colias eriphyle to repeated exposure to high,sub‐lethal temperatures

The optimal temperature at which an organism grows and develops is commonly correlated with latitude and elevation; however, the maximum temperature for physiological performance often is not. This makes performance at temperatures between the optimum and the maximum of particular interest. Temperature can influence long‐term performance (growth and development), as well as short‐term performance (heat shock protein) responses differentially. In the present study, two populations of the clouded sulphur butterfly Colias eriphyle Edwards that differ in elevation, thermal regime and optimal and maximum temperatures are studied to quantify their responses to repeated, sub‐lethal heat treatments early in development (second instar). Heat treatments accelerate development during the second to fourth instars in both populations initially, although this effect disappears by pupation. Heat treatment decreases pupal mass in the lower elevation population, suggesting that repeated exposure to high temperatures early in development may reduce final size and fecundity in this population. Heat shock protein gene (hsp70) expression levels in the lower elevation (1633 m a.s.l.) population are highest 24 h after the start of the heat treatment and then the fall to pre‐exposure levels by 36–72 h, suggesting a rapid response to stressful temperatures. By contrast, heat treatment has no significant effect on pupal mass in the higher elevation (2347 m a.s.l.) population. This population has higher levels of hsp70 expression overall but constant expression levels, suggesting that the temperature treatments used are insufficient to elicit a heat stress response. Overall, the effects of repeated exposure to sub‐lethal high temperatures early in development on growth, final size and gene expression differ between populations that differ in thermal sensitivity.     

Effects of experimental warming on survival,phenology, and morphology of an aquatic insect (Odonata)

1. Organisms can respond to changing climatic conditions in multiple ways including changes in phenology, body size or morphology, and range shifts. Understanding how developmental temperatures affect insect life‐history timing and morphology is crucial because body size and morphology affect multiple aspects of life history, including dispersal ability, whereas phenology can shape population performance and community interactions. 2. It was experimentally assessed how developmental temperatures experienced by aquatic larvae affected survival, phenology, and adult morphology of dragonflies [Pachydiplax longipennis (Burmeister)]. Larvae were reared under three environmental temperatures: ambient, +2.5, and +5 °C, corresponding to temperature projections for our study area 50 and 100 years in the future, respectively. Experimental temperature treatments tracked naturally‐occurring variation. 3. Clear effects of temperature were found in the rearing environment on survival and phenology: dragonflies reared at the highest temperatures had the lowest survival rates and emerged from the larval stage approximately 3 weeks earlier than animals reared at ambient temperatures. There was no effect of rearing temperature on overall body size. Although neither the relative wing nor thorax size was affected by warming, a non‐significant trend towards an interaction between sex and warming in relative thorax size suggests that males may be more sensitive to warming than females, a pattern that should be investigated further. 4. Warming strongly affected survival in the larval stage and the phenology of adult emergence. Understanding how warming in the developmental environment affects later life‐history stages is critical to interpreting the consequences of warming for organismal performance.     

The endemic kelp Lessonia corrugata is being pushed above its thermal limits in an ocean warming hotspot

Kelps are in global decline due to climate change, which includes ocean warming. To identify vulnerable species, we need to identify their tolerances to increasing temperatures and determine whether tolerances are altered by co-occurring drivers such as inorganic nutrient levels. This is particularly important for those species with restricted distributions, which may already be experiencing thermal stress. To identify thermal tolerance of the range-restricted kelp Lessonia corrugata, we conducted a laboratory experiment on juvenile sporophytes to measure performance (growth, photosynthesis) across its thermal range (4–22°C). We determined the upper thermal limit for growth and photosynthesis to be ~22–23°C, with a thermal optimum of ~16°C. To determine if elevated inorganic nitrogen availability could enhance thermal tolerance, we compared the performance of juveniles under low (4.5 μmol · d⁻¹) and high (90 μmol · d⁻¹) nitrate conditions at and above the thermal optimum (16–23.5°C). Nitrate enrichment did not enhance thermal performance at temperatures above the optimum but did lead to elevated growth rates at the thermal optimum. Our results indicate L. corrugata is likely to be extremely susceptible to moderate ocean warming and marine heatwaves. Peak sea surface temperatures during summer in eastern and northeastern Tasmania can reach up to 20–21°C, and climate projections suggest that L. corrugata's thermal limit will be regularly exceeded by 2050 as southeastern Australia is a global ocean-warming hotspot. By identifying the upper thermal limit of L. corrugata, we have taken a critical step in predicting the future of the species in a warming climate.     

Hyperkalaemia,not apoptosis,accurately predicts insect chilling injury

There is a growing appreciation that insect distribution and abundance are associated with the limits of thermal tolerance, but the physiology underlying thermal tolerance remains poorly understood. Many insects, like the migratory locust (Locusta migratoria), suffer a loss of ion and water balance leading to hyperkalaemia (high extracellular [K⁺]) in the cold that indirectly causes cell death. Cells can die in several ways under stress, and how they die is of critical importance to identifying and understanding the nature of thermal adaptation. Whether apoptotic or necrotic cell death pathways are responsible for low-temperature injury is unclear. Here, we use a caspase-3 specific assay to indirectly quantify apoptotic cell death in three locust tissues (muscle, nerves and midgut) following prolonged chilling and recovery from an injury-inducing cold exposure. Furthermore, we obtain matching measurements of injury, extracellular [K⁺] and muscle caspase-3 activity in individual locusts to gain further insight into the mechanistic nature of chilling injury. We found a significant increase in muscle caspase-3 activity, but no such increase was observed in either nervous or gut tissue from the same animals, suggesting that chill injury primarily relates to muscle cell death. Levels of chilling injury measured at the whole animal level, however, were strongly correlated with the degree of haemolymph hyperkalaemia, and not apoptosis. These results support the notion that cold-induced ion balance disruption triggers cell death but also that apoptosis is not the main form of cell damage driving low-temperature injury.