Heat resistance throughout ontogeny: body size constrains thermal tolerance

Heat tolerance is a trait of paramount ecological importance and may determine a species' ability to cope with ongoing climate change. Although critical thermal limits have consequently received substantial attention in recent years, their potential variation throughout ontogeny remained largely neglected. We investigate whether such neglect may bias conclusions regarding a species' sensitivity to climate change. Using a tropical butterfly, we found that developmental stages clearly differed in heat tolerance. It was highest in pupae followed by larvae, adults and finally eggs and hatchlings. Strikingly, most of the variation found in thermal tolerance was explained by differences in body mass, which may thus impose a severe constraint on adaptive variation in stress tolerance. Furthermore, temperature acclimation was beneficial by increasing heat knock‐down time and therefore immediate survival under heat stress, but it affected reproduction negatively. Extreme temperatures strongly reduced survival and subsequent reproductive success even in our highly plastic model organism, exemplifying the potentially dramatic impact of extreme weather events on biodiversity. We argue that predictions regarding a species' fate under changing environmental conditions should consider variation in thermal tolerance throughout ontogeny, variation in body mass and acclimation responses as important predictors of stress tolerance.     

Plasticity and cross‐tolerance to heterogeneous environments: divergent stress responses co‐evolved in an African fruit fly

Plastic adjustments of physiological tolerance to a particular stressor can result in fitness benefits for resistance that might manifest not only in that same environment but also be advantageous when faced with alternative environmental stressors, a phenomenon termed ‘cross‐tolerance’. The nature and magnitude of cross‐tolerance responses can provide important insights into the underlying genetic architecture, potential constraints on or versatility of an organism's stress responses. In this study, we tested for cross‐tolerance to a suite of abiotic factors that likely contribute to setting insect population dynamics and geographic range limits: heat, cold, desiccation and starvation resistance in adult Ceratitis rosa following acclimation to all these isolated individual conditions prior to stress assays. Traits of stress resistance scored included critical thermal (activity) limits, chill coma recovery time (CCRT), heat knockdown time (HKDT), desiccation and starvation resistance. In agreement with other studies, we found that acclimation to one stress typically increased resistance for that same stress experienced later in life. A more novel outcome, however, is that here we also found substantial evidence for cross‐tolerance. For example, we found an improvement in heat tolerance (critical thermal maxima, CT_max) following starvation or desiccation hardening and improved desiccation resistance following cold acclimation, indicating pronounced cross‐tolerance to these environmental stressors for the traits examined. We also found that two different traits of the same stress resistance differed in their responsiveness to the same stress conditions (e.g. HKDT was less cross‐resistant than CT_max). The results of this study have two major implications that are of broader importance: (i) that these traits likely co‐evolved to cope with diverse or simultaneous stressors, and (ii) that a set of common underlying physiological mechanisms might exist between apparently divergent stress responses in this species. This species may prove to be a valuable model for future work on the evolutionary and mechanistic basis of cross‐tolerance.     

Plasticity and local adaptation explain lizard cold tolerance

How does climate variation limit the range of species and what does it take for species to colonize new regions? In this issue of Molecular Ecology, Campbell‐Staton et al. ( 2018 ) address these broad questions by investigating cold tolerance adaptation in the green anole lizard (Anolis carolinensis) across a latitudinal transect. By integrating physiological data, gene expression data and acclimation experiments, the authors disentangle the mechanisms underlying cold adaptation. They first establish that cold tolerance adaptation in Anolis lizards follows the predictions of the oxygen‐ and capacity‐limited thermal tolerance hypothesis, which states that organisms are limited by temperature thresholds at which oxygen supply cannot meet demand. They then explore the drivers of cold tolerance at a finer scale, finding evidence that northern populations are adapted to cooler thermal regimes and that both phenotypic plasticity and heritable genetic variation contribute to cold tolerance. The integration of physiological and gene expression data further highlights the varied mechanisms that drive cold tolerance adaptation in Anolis lizards, including both supply‐side and demand‐side adaptations that improve oxygen economy. Altogether, their work provides new insight into the physiological and genetic mechanisms underlying adaptation to new climatic niches and demonstrates that cold tolerance in northern lizard populations is achieved through the synergy of physiological plasticity and local genetic adaptation for thermal performance.     

Evolutionary and environmental determinants of freshwater fish thermal tolerance and plasticity

Understanding the extent to which phylogenetic constraints and adaptive evolutionary forces help define the physiological sensitivity of species is critical for anticipating climate‐related impacts in aquatic environments. Yet, whether upper thermal tolerance and plasticity are shaped by common evolutionary and environmental mechanisms remains to be tested. Based on a systematic literature review, we investigated this question in 82 freshwater fish species (27 families) representing 829 experiments for which data existed on upper thermal limits and it was possible to estimate plasticity using upper thermal tolerance reaction norms. Our findings indicated that there are strong phylogenetic signals in both thermal tolerances and acclimation capacity, although it is weaker in the latter. We found that upper thermal tolerances are correlated with the temperatures experienced by species across their range, likely because of spatially autocorrelated processes in which closely related species share similar selection pressures and limited dispersal from ancestral environments. No association with species thermal habitat was found for acclimation capacity. Instead, species with the lowest physiological plasticity also displayed the highest thermal tolerances, reflecting to some extent an evolutionary trade‐off between these two traits. Although our study demonstrates that macroecological climatic niche features measured from species distributions are likely to provide a good approximation of freshwater fish sensitivity to climate change, disentangling the mechanisms underlying both acute and chronic heat tolerances may help to refine predictions regarding climate change‐related range shifts and extinctions.     

Lethal and sublethal behavioural responses of saline water beetles to acute heat and osmotic stress

1. As species' physiological breadth determines their potential to deal with environmental changes, and influences individuals' survival and the persistence of populations, information about lethal and sublethal responses could be fundamental for conservation purposes. 2. We used a standard experimental approach to explore mortality and behavioural avoidance responses (i.e. flight and emersion from the water) to a combination of acute heat and osmotic stress on six species of saline water beetles (belonging to Enochrus, Nebrioporus, and Ochthebius genera). 3. Heat stress affected survival and behavioural responses in all of the species, whereas osmotic stress and the interaction between both stressors only showed significant effects for the Ochthebius genus. Behavioural and survival patterns were highly interrelated across the stress gradients. The Enochrus and Nebrioporus studied species showed maximum avoidance activity at 35–40 °C, and a short (< 30 min) exposure to 45 °C was lethal. Ochthebius species were the most heat tolerant and displayed increasing behavioural responses with increasing temperature. In the Nebrioporus and Ochthebius genera, the species occupying lotic, more environmentally stable habitats, showed greater mortality, and avoidance responses were higher or initiated at lower stress thresholds than lentic species. In contrast, both Enochrus species displayed a similar mortality, and the lentic species E. bicolor emerged and flew more than the lotic E. falcarius, in concordance with its higher dispersal capacity. 4. Avoidance responses could provide interesting information about species' physiological amplitudes as a complement to lethal responses. The lotic species here studied showed narrower physiological amplitude (i.e. N. baeticus and O. glaber) or lower dispersal ability (i.e. E. falcarius) than their lentic relatives; both traits could result in a higher vulnerability of lotic species to thermal habitat changes.     

Global variation in thermal tolerances and vulnerability of endotherms to climate change

The relationships among species'' physiological capacities and the geographical variation of ambient climate are of key importance to understanding the distribution of life on the Earth. Furthermore, predictions of how species will respond to climate change will profit from the explicit consideration of their physiological tolerances. The climatic variability hypothesis, which predicts that climatic tolerances are broader in more variable climates, provides an analytical framework for studying these relationships between physiology and biogeography. However, direct empirical support for the hypothesis is mostly lacking for endotherms, and few studies have tried to integrate physiological data into assessments of species'' climatic vulnerability at the global scale. Here, we test the climatic variability hypothesis for endotherms, with a comprehensive dataset on thermal tolerances derived from physiological experiments, and use these data to assess the vulnerability of species to projected climate change. We find the expected relationship between thermal tolerance and ambient climatic variability in birds, but not in mammals—a contrast possibly resulting from different adaptation strategies to ambient climate via behaviour, morphology or physiology. We show that currently most of the species are experiencing ambient temperatures well within their tolerance limits and that in the future many species may be able to tolerate projected temperature increases across significant proportions of their distributions. However, our findings also underline the high vulnerability of tropical regions to changes in temperature and other threats of anthropogenic global changes. Our study demonstrates that a better understanding of the interplay among species'' physiology and the geography of climate change will advance assessments of species'' vulnerability to climate change.     

Cold tolerance of the invasive Carcinus maenas in the east Pacific: molecular mechanisms and implications for range expansion in a changing climate

Physiological studies have long been utilized to understand the role of environmental temperature in the distribution of native organisms within marine communities. For the invasive crab Carcinus maenas, temperature has been implicated as the main predictor of establishment success across temperate regions. Therefore, we determined whether the lower temperature tolerances of this non-native crab would restrict it from spreading farther poleward from a relatively new recipient environment. Cold tolerance capacity was determined in the laboratory by holding crabs sampled from Vancouver Island, British Columbia (BC)—near the present northern limit for the northeast Pacific metapopulation to an overwintering thermal profile generated from Sitka, Alaska, USA. These crabs were physiologically capable of overwintering north of their present range boundary. The cellular response to cold stress was investigated using two functional categories of the cellular stress response. We measured cyclin D1, a cell-cycle regulator, and Hsp70, a protein chaperone, after laboratory acclimation and acute cold stress on two populations of C. maenas from the west coast of North America that have disparate thermal histories (crabs sampled from CA or BC). We found site-specific differential expression of cyclin D1 after cold acclimation and cold shock, perhaps affecting invasion capacity in this species. Determining what physiological mechanisms are in place with respect to thermal tolerance and preference can give insight into what makes an invasive organism successful and aid in predicting probable distribution of such species within a new environment.     

Linking species thermal tolerance to elevational range shifts in upland dung beetles

Climate warming has been proposed as the main cause of the recent range shifts seen in many species. Although species' thermal tolerances are thought to play a key role in determining responses to climate change, especially in ectotherms, empirical evidence is still limited. We investigate the connection between species' thermal tolerances, elevational range and shifts in the lower elevational limit of dung beetle species (Coleoptera, Aphodiidea) in an upland region in the northwest of England. We measured thermal tolerances in the laboratory, and used current and historical distribution data to test specific hypotheses about the area's three dominant species, particularly the species most likely to suffer from warming: Agollinus lapponum. We found marked differences between species in their minimum and maximum thermal tolerance and in their elevational range and patterns of abundance. Overall, differences in thermal limits among species matched the abundance patterns along the elevation gradient expected if distributions were constrained by climate. Agollinus lapponum abundance increased with elevation and this species showed lower maximum and minimum thermal limits than Acrossus depressus, for which abundance declined with elevation. Consistent with lower tolerance to high temperature, we recorded an uphill retreat of the low elevation limit of A. lapponum (177 m over 57 yr) in line with the increase in summer temperature observed in the region over the same period. Moreover, this species has been replaced at low and mid‐elevations by the other two warm‐tolerant species (A. depressus and Agrilinus ater). Our results provide empirical evidence that species' thermal tolerance constrains elevational ranges and contributes to explain the observed responses to climate warming. A mechanistic understanding of how climate change directly affects species, such as the one presented here, will provide a robust base to inform predictions of how individual species and whole assemblages may change in the future.     

Extensive Acclimation in Ectotherms Conceals Interspecific Variation in Thermal Tolerance Limits

Species’ tolerance limits determine their capacity to tolerate climatic extremes and limit their potential distributions. Interspecific variation in thermal tolerances is often proposed to indicate climatic vulnerability and is, therefore, the subject of many recent meta-studies on differential capacities of species from climatically different habitats to deal with climate change. Most studies on thermal tolerances do not acclimate animals or use inconsistent, and insufficient, acclimation times, limiting our knowledge of the shape, duration and extent of acclimation responses. Consequently patterns in thermal tolerances observed in meta-analyses, based on data from the literature are based on inconsistent, partial acclimation and true trends may be obscured. In this study we describe time-course of complete acclimation of critical thermal minima in the tropical ectotherm Carlia longipes and compare it to the average acclimation response of other reptiles, estimated from published data, to assess how much acclimation time may contribute to observed differences in thermal limits. Carlia longipes decreased their lower critical thermal limits by 2.4°C and completed 95% of acclimation in 17 weeks. Wild populations did not mirror this acclimation process over the winter. Other reptiles appear to decrease cold tolerance more quickly (95% in 7 weeks) and to a greater extent, with an estimated average acclimation response of 6.1°C. However, without data on tolerances after longer acclimation times available, our capacity to estimate final acclimation state is very limited. Based on the subset of data available for meta-analysis, much of the variation in cold tolerance observed in the literature can be attributed to acclimation time. Our results indicate that (i) acclimation responses can be slow and substantial, even in tropical species, and (ii) interspecific differences in acclimation speed and extent may obscure trends assessed in some meta-studies. Cold tolerances of wild animals are representative of cumulative responses to recent environments, while lengthy acclimation is necessary for controlled comparisons of physiological tolerances. Measures of inconsistent, intermediate acclimation states, as reported by many studies, represent neither the realised nor the potential tolerance in that population, are very likely underestimates of species’ physiological capacities and may consequently be of limited value.     

Moving forward in global‐change ecology: capitalizing on natural variability

Natural resources managers are being asked to follow practices that accommodate for the impact of climate change on the ecosystems they manage, while global‐ecosystems modelers aim to forecast future responses under different climate scenarios. However, the lack of scientific knowledge about short‐term ecosystem responses to climate change has made it difficult to define set conservation practices or to realistically inform ecosystem models. Until recently, the main goal for ecologists was to study the composition and structure of communities and their implications for ecosystem function, but due to the probable magnitude and irreversibility of climate‐change effects (species extinctions and loss of ecosystem function), a shorter term focus on responses of ecosystems to climate change is needed. We highlight several underutilized approaches for studying the ecological consequences of climate change that capitalize on the natural variability of the climate system at different temporal and spatial scales. For example, studying organismal responses to extreme climatic events can inform about the resilience of populations to global warming and contribute to the assessment of local extinctions. Translocation experiments and gene expression are particular useful to quantitate a species' acclimation potential to global warming. And studies along environmental gradients can guide habitat restoration and protection programs by identifying vulnerable species and sites. These approaches identify the processes and mechanisms underlying species acclimation to changing conditions, combine different analytical approaches, and can be used to improve forecasts of the short‐term impacts of climate change and thus inform conservation practices and ecosystem models in a meaningful way.     

Limited plasticity of low temperature tolerance in an Australian cantharid beetle Chauliognathus lugubris

Spatial and/or taxonomic bias in thermal tolerance and plasticity data can severely impact projections of climate change responses and limit the understanding of the evolution of thermal performance curves. Thus, further data from under‐represented groups and geographical locations are important for synthesizing and predicting the physiological responses of insects to climate variability. For example, the magnitude of rapid cold‐hardening (RCH) and seasonal acclimatization of low temperature tolerance are typically poorly documented for nondipteran species from the southern Hemisphere. Moreover, few studies assess RCH responses under different acclimation regimes. To address this paucity of data, the low temperature survival, RCH and acclimation ability of Chauliognathus lugubris (F.) are assessed from an adult aggregation collected in Armidale, New South Wales, Australia. Beetles are acclimated to either 27 or 20 °C for 1 week and then tested for their ability to survive cold shock or rapidly cold‐harden. There is no effect of acclimation on low temperature survival (mean survival range at ?5.4 °C for 2 h: 4–52% in 27 and 20 °C acclimation groups). In addition, beetles show no significant improvement in survival after acute thermal pretreatments. In conclusion, these data suggest a generally poor acclimation potential of low temperature survival and no RCH responses in adult Australian cantharid beetles, which is accordance with what might be expected given the microclimate experienced, their ability for behavioural regulation and the life history of the species.     

Physical effects of habitat‐forming species override latitudinal trends in temperature

Latitudinal and elevational temperature gradients (LTG and ETG) play central roles in biogeographical theory, underpinning predictions of large‐scale patterns in organismal thermal stress, species' ranges and distributional responses to climate change. Yet an enormous fraction of Earth's taxa live exclusively in habitats where foundation species modify temperatures. We examine little‐explored implications of this widespread trend using a classic model system for understanding heat stresses – rocky intertidal shores. Through integrated field measurements and laboratory trials, we demonstrate that thermal buffering by centimetre‐thick mussel and seaweed beds eliminates differences in stress‐inducing high temperatures and associated mortality risk that would otherwise arise over 14° of latitude and ~ 1 m of shore elevation. These results reveal the extent to which physical effects of habitat‐formers can overwhelm broad‐scale thermal trends, suggesting a need to re‐evaluate climate change predictions for many species. Notably, inhabitant populations may exhibit deceptive resilience to warming until refuge‐forming taxa become imperiled.     

Advances in understanding the impacts of global warming on marine fishes farmed offshore: Sparus aurata as a case study

Monitoring variations in proteins involved in metabolic processes, oxidative stress responses, cell signalling and protein homeostasis is a powerful tool for developing hypotheses of how environmental variations affect marine organisms' physiology and biology. According to the oxygen- and capacity-limited thermal tolerance hypothesis, thermal acclimation mechanisms such as adjusting the activities of enzymes of intermediary metabolism and of antioxidant defence mechanisms, inducing heat shock proteins (Hsps) or activating mitogen-activated protein kinases may all shift tolerance windows. Few studies have, however, investigated the molecular, biochemical and organismal responses by fishes to seasonal temperature variations in the field to link these to laboratory findings. Investigation of the impacts of global warming on fishes farmed offsore, in the open sea, can provide a stepping stone towards understanding effects on wild populations because they experience similar environmental fluctuations. Over the last 30 years, farming of the gilthead sea bream Sparus aurata (Linnaeus 1758) has become widespread along the Mediterranean coastline, rendering this species a useful case study. Based on available information, the prevailing seasonal temperature variations expose the species to the upper and lower limits of its thermal range. Evidence for this includes oxygen restriction, reduced feeding, reduced responsiveness to environmental stimuli, plus a range of molecular and biochemical indicators that change across the thermal range. Additionally, close relationships between biochemical pathways and seasonal patterns of metabolism indicate a connection between energy demand and metabolic processes on the one hand, and cellular stress responses such as oxidative stress, inflammation and autophagy on the other. Understanding physiological responses to temperature fluctuations in fishes farmed offshore can provide crucial background information for the conservation and successful management of aquaculture resources in the face of global change.     

Sub-lethal temperature thresholds indicate acclimation and physiological limits in brook trout Salvelinus fontinalis

The upper thermal tolerance of brook trout Salvelinus fontinalis was estimated using critical thermal maxima (CT_max) experiments on fish acclimated to temperatures that span the species' thermal range (5–25°C). The CT_max increased with acclimation temperature but plateaued in fish acclimated to 20, 23 and 25°C. Plasma lactate was highest, and the hepato-somatic index (I_H) was lowest at 23 and 25°C, which suggests additional metabolic costs at those acclimation temperatures. The results suggest that there is a sub-lethal threshold between 20 and 23°C, beyond which the fish experience reduced physiological performance.     

Historical and event‐based bioclimatic suitability predicts regional forest vulnerability to compound effects of severe drought and bark beetle infestation

Vulnerability to climate change, and particularly to climate extreme events, is expected to vary across species ranges. Thus, we need tools to standardize the variability in regional climatic legacy and extreme climate across populations and species. Extreme climate events (e.g., droughts) can erode populations close to the limits of species' climatic tolerance. Populations in climatic‐core locations may also become vulnerable because they have developed a greater demand for resources (i.e., water) that cannot be enough satisfied during the periods of scarcity. These mechanisms can become exacerbated in tree populations when combined with antagonistic biotic interactions, such as insect infestation. We used climatic suitability indices derived from Species Distribution Models (SDMs) to standardize the climatic conditions experienced across Pinus edulis populations in southwestern North America, during a historical period (1972–2000) and during an extreme event (2001–2007), when the compound effect of hot drought and bark beetle infestation caused widespread die‐off and mortality. Pinus edulis climatic suitability diminished dramatically during the die‐off period, with remarkable variation between years. P. edulis die‐off occurred mainly not just in sites that experienced lower climatic suitability during the drought but also where climatic suitability was higher during the historical period. The combined effect of historically high climatic suitability and a marked decrease in the climatic suitability during the drought best explained the range‐wide mortality. Lagged effects of climatic suitability loss in previous years and co‐occurrence of Juniperus monosperma also explained P. edulis die‐off in particular years. Overall, the study shows that past climatic legacy, likely determining acclimation, together with competitive interactions plays a major role in responses to extreme drought. It also provides a new approach to standardize the magnitude of climatic variability across populations using SDMs, improving our capacity to predict population's or species' vulnerability to climatic change.     

Seasonal variation in basal and plastic cold tolerance: Adaptation is influenced by both long‐ and short‐term phenotypic plasticity

Understanding how thermal selection affects phenotypic distributions across different time scales will allow us to predict the effect of climate change on the fitness of ectotherms. We tested how seasonal temperature variation affects basal levels of cold tolerance and two types of phenotypic plasticity in Drosophila melanogaster. Developmental acclimation occurs as developmental stages of an organism are exposed to seasonal changes in temperature and its effect is irreversible, while reversible short‐term acclimation occurs daily in response to diurnal changes in temperature. We collected wild flies from a temperate population across seasons and measured two cold tolerance metrics (chill‐coma recovery and cold stress survival) and their responses to developmental and short‐term acclimation. Chill‐coma recovery responded to seasonal shifts in temperature, and phenotypic plasticity following both short‐term and developmental acclimation improved cold tolerance. This improvement indicated that both types of plasticity are adaptive, and that plasticity can compensate for genetic variation in basal cold tolerance during warmer parts of the season when flies tend to be less cold tolerant. We also observed a significantly stronger trade‐off between basal cold tolerance and short‐term acclimation during warmer months. For the longer‐term developmental acclimation, a trade‐off persisted regardless of season. A relationship between the two types of plasticity may provide additional insight into why some measures of thermal tolerance are more sensitive to seasonal variation than others.     

Wrong place,wrong time: climate change‐induced range shift across fragmented habitat causes maladaptation and declined population size in a modelled bird species

Many species are locally adapted to decreased habitat quality at their range margins, and therefore show genetic differences throughout their ranges. Under contemporary climate change, range shifts may affect evolutionary processes at the expanding range margin due to founder events. In addition, populations that are affected by such founder events will, in the course of time, become located in the range centre. Recent studies investigated evolutionary changes at the expanding range margin, but have not assessed eventual effects across the species' range. We explored the possible influence of range shift on the level of adaptation throughout the species' total range. For this we used a spatially explicit, individual‐based simulation model of a woodland bird, parameterized after the middle spotted woodpecker ( Dendrocopos medius) in fragmented habitat. We simulated its range under climate change, and incorporated genetic differences at a single locus that determined the individual's degree of adaptation to optimal temperature conditions. Generalist individuals had a large thermal tolerance, but relatively low overall fitness, whereas climate specialists had high fitness combined with a small thermal tolerance. In equilibrium, the populations in the range centre were comprised of the specialists, whereas the generalists dominated the margins. In contrast, under temperature increase, the generalist numbers increased at the expanding margin and eventually also occupied the centre of the shifting range, whereas the specialists were located in the retracting margins. This was caused by founder events and led to overall maladaptation of the species, which resulted in a reduced metapopulation size and thus impeded the species' persistence. We therefore found no evidence for a complementary effect of local adaptation and range shifts on species' survival. Instead, we showed that founder events can cause local maladaptation which can amplify throughout the species' range, and, as such, hamper the species' persistence under climate change.