Hydric effects on thermal tolerances influence climate vulnerability in a high-latitude beetle

Species' thermal tolerances are used to estimate climate vulnerability, but few studies consider the role of the hydric environment in shaping thermal tolerances. As environments become hotter and drier, organisms often respond by limiting water loss to lower the risk of desiccation; however, reducing water loss may produce trade-offs that lower thermal tolerances if respiration becomes inhibited. Here, we measured the sensitivity of water loss rate and critical thermal maximum (CT_max) to precipitation in nature and laboratory experiments that exposed click beetles (Coleoptera: Elateridae) to acute- and long-term humidity treatments. We also took advantage of their unique clicking behavior to characterize subcritical thermal tolerances. We found higher water loss rates in the dry acclimation treatment compared to the humid, and water loss rates were 3.2-fold higher for individuals that had experienced a recent precipitation event compared to individuals that had not. Acute humidity treatments did not affect CT_max, but precipitation indirectly affected CT_max through its effect on water loss rates. Contrary to our prediction, we found that CT_max was negatively associated with water loss rate, such that individuals with high water loss rate exhibited a lower CT_max. We then incorporated the observed variation of CT_max into a mechanistic niche model that coupled leaf and click beetle temperatures to predict climate vulnerability. The simulations indicated that indices of climate vulnerability can be sensitive to the effects of water loss physiology on thermal tolerances; moreover, exposure to temperatures above subcritical thermal thresholds is expected to increase by as much as 3.3-fold under future warming scenarios. The correlation between water loss rate and CT_max identifies the need to study thermal tolerances from a “whole-organism” perspective that considers relationships between physiological traits, and the population-level variation in CT_max driven by water loss rate complicates using this metric as a straightforward proxy of climate vulnerability.     

Disparate patterns of thermal adaptation between life stages in temperate vs. tropical Drosophila melanogaster

Many terrestrial ectothermic species exhibit limited variation in upper thermal tolerance across latitude. However, these trends may not signify limited adaptive capacity to increase thermal tolerance in the face of climate change. Instead, thermal tolerance may be similar among populations because behavioural thermoregulation by mobile organisms or life stages may buffer natural selection for thermal tolerance. We compared thermal tolerance of adults and embryos among natural populations of Drosophila melanogaster from a broad range of thermal habitats around the globe to assess natural variation of thermal tolerance in mobile vs. immobile life stages. We found no variation among populations in adult thermal tolerance, but embryonic thermal tolerance was higher in tropical strains than in temperate strains. We further report that embryos live closer to their upper thermal limits than adults – that is, thermal safety margins are smaller for embryos than adults. F1 hybrid embryos from crosses between temperate and tropical populations had thermal tolerance that matched that of tropical embryos, suggesting the dominance of heat‐tolerant alleles. Together, our findings suggest that thermal selection has led to divergence in embryonic thermal tolerance but that selection for divergent thermal tolerance may be limited in adults. Further, our results suggest that thermal traits should be measured across life stages to better predict adaptive limits.     

Heat tolerance of marine ectotherms in a warming Antarctica

Global warming is affecting the Antarctic continent in complex ways. Because Antarctic organisms are specialized to living in the cold, they are vulnerable to increasing temperatures, although quantitative analyses of this issue are currently lacking. Here we compiled a total of 184 estimates of heat tolerance belonging to 39 marine species and quantified how survival is affected concomitantly by the intensity and duration of thermal stress. Species exhibit thermal limits displaced toward colder temperatures, with contrasting strategies between arthropods and fish that exhibit low tolerance to acute heat challenges, and brachiopods, echinoderms, and molluscs that tend to be more sensitive to chronic exposure. These differences might be associated with mobility. A dynamic mortality model suggests that Antarctic organisms already encounter temperatures that might be physiologically stressful and indicate that these ecological communities are indeed vulnerable to ongoing rising temperatures.     

Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming

Global warming is increasing the overheating risk for many organisms, though the potential for plasticity in thermal tolerance to mitigate this risk is largely unknown. In part, this shortcoming stems from a lack of knowledge about global and taxonomic patterns of variation in tolerance plasticity. To address this critical issue, we test leading hypotheses for broad-scale variation in ectotherm tolerance plasticity using a dataset that includes vertebrate and invertebrate taxa from terrestrial, freshwater and marine habitats. Contrary to expectation, plasticity in heat tolerance was unrelated to latitude or thermal seasonality. However, plasticity in cold tolerance is associated with thermal seasonality in some habitat types. In addition, aquatic taxa have approximately twice the plasticity of terrestrial taxa. Based on the observed patterns of variation in tolerance plasticity, we propose that limited potential for behavioural plasticity (i.e. behavioural thermoregulation) favours the evolution of greater plasticity in physiological traits, consistent with the ‘Bogert effect’. Finally, we find that all ectotherms have relatively low acclimation in thermal tolerance and demonstrate that overheating risk will be minimally reduced by acclimation in even the most plastic groups. Our analysis indicates that behavioural and evolutionary mechanisms will be critical in allowing ectotherms to buffer themselves from extreme temperatures.     

Freshwater species distributions along thermal gradients

The distribution of a species along a thermal gradient is commonly approximated by a unimodal response curve, with a characteristic single optimum near the temperature where a species is most likely to be found, and a decreasing probability of occurrence away from the optimum. We aimed at identifying thermal response curves (TRCs) of European freshwater species and evaluating the potential impact of climate warming across species, taxonomic groups, and latitude. We first applied generalized additive models using catchment‐scale global data on distribution ranges of 577 freshwater species native to Europe and four different temperature variables (the current annual mean air/water temperature and the maximum air/water temperature of the warmest month) to describe species TRCs. We then classified TRCs into one of eight curve types and identified spatial patterns in thermal responses. Finally, we integrated empirical TRCs and the projected geographic distribution of climate warming to evaluate the effect of rising temperatures on species’ distributions. For the different temperature variables, 390–463 of 577 species (67.6%–80.2%) were characterized by a unimodal TRC. The number of species with a unimodal TRC decreased from central toward northern and southern Europe. Warming tolerance (WT = maximum temperature of occurrence—preferred temperature) was higher at higher latitudes. Preferred temperature of many species is already exceeded. Rising temperatures will affect most Mediterranean species. We demonstrated that freshwater species’ occurrence probabilities are most frequently unimodal. The impact of the global climate warming on species distributions is species and latitude dependent. Among the studied taxonomic groups, rising temperatures will be most detrimental to fish. Our findings support the efforts of catchment‐based freshwater management and conservation in the face of global warming.     

Occupancy‐derived thermal affinities reflect known physiological thermal limits of marine species

Predicting how species will respond to increased environmental temperatures is key to understanding the ecological consequences of global change. The physiological tolerances of a species define its thermal limits, while its thermal affinity is a summary of the environmental temperatures at the localities at which it actually occurs. Experimentally derived thermal limits are known to be related to observed latitudinal ranges in marine species, but accurate range maps from which to derive latitudinal ranges are lacking for many marine species. An alternative approach is to combine widely available data on global occurrences with gridded global temperature datasets to derive measures of species‐level “thermal affinity”—that is, measures of the central tendency, variation, and upper and lower bounds of the environmental temperatures at the locations at which a species has been recorded to occur. Here, we test the extent to which such occupancy‐derived measures of thermal affinity are related to the known thermal limits of marine species using data on 533 marine species from 24 taxonomic classes and with experimentally derived critical upper temperatures spanning 2–44.5°C. We show that thermal affinity estimates are consistently and positively related to the physiological tolerances of marine species, despite gaps and biases in the source data. Our method allows thermal affinity measures to be rapidly and repeatably estimated for many thousands more marine species, substantially expanding the potential to assess vulnerability of marine communities to warming seas.     

Thermal tolerance and climate warming sensitivity in tropical snails

Tropical ectotherms are predicted to be especially vulnerable to climate change because their thermal tolerance limits generally lie close to current maximum air temperatures. This prediction derives primarily from studies on insects and lizards and remains untested for other taxa with contrasting ecologies. We studied the HCT (heat coma temperatures) and ULT (upper lethal temperatures) of 40 species of tropical eulittoral snails (Littorinidae and Neritidae) inhabiting exposed rocky shores and shaded mangrove forests in Oceania, Africa, Asia and North America. We also estimated extremes in animal body temperature at each site using a simple heat budget model and historical (20 years) air temperature and solar radiation data. Phylogenetic analyses suggest that HCT and ULT exhibit limited adaptive variation across habitats (mangroves vs. rocky shores) or geographic locations despite their contrasting thermal regimes. Instead, the elevated heat tolerance of these species (HCT = 44.5 ± 1.8°C and ULT = 52.1 ± 2.2°C) seems to reflect the extreme temperature variability of intertidal systems. Sensitivity to climate warming, which was quantified as the difference between HCT or ULT and maximum body temperature, differed greatly between snails from sunny (rocky shore; Thermal Safety Margin, TSM = −14.8 ± 3.3°C and −6.2 ± 4.4°C for HCT and ULT, respectively) and shaded (mangrove) habitats (TSM = 5.1 ± 3.6°C and 12.5 ± 3.6°C). Negative TSMs in rocky shore animals suggest that mortality is likely ameliorated during extreme climatic events by behavioral thermoregulation. Given the low variability in heat tolerance across species, habitat and geographic location account for most of the variation in TSM and may adequately predict the vulnerability to climate change. These findings caution against generalizations on the impact of global warming across ectothermic taxa and highlight how the consideration of nonmodel animals, ecological transitions, and behavioral responses may alter predictions of studies that ignore these biological details.     

A framework for integrating thermal biology into fragmentation research

Habitat fragmentation changes thermal conditions in remnant patches, and thermal conditions strongly influence organism morphology, distribution, and activity patterns. However, few studies explore temperature as a mechanism driving ecological responses to fragmentation. Here we offer a conceptual framework that integrates thermal biology into fragmentation research to better understand individual, species, community, and ecosystem‐level responses to fragmentation. Specifically, the framework addresses how fragmentation changes temperature and how the effects of those temperature changes spread through the ecosystem, from organism response via thermal sensitivity, to changes in species distribution and activity patterns, to shifts in community structure following species' responses, and ultimately to changes in ecosystem functions. We place a strong emphasis on future research directions by outlining “Critical gaps” for each step of the framework. Empirical efforts to apply and test this framework promise new understanding of fragmentation's ecological consequences and new strategies for conservation in an increasingly fragmented and warmer world.     

Adaptation to simultaneous warming and acidification carries a thermal tolerance cost in a marine copepod

The ocean is undergoing warming and acidification. Thermal tolerance is affected both by evolutionary adaptation and developmental plasticity. Yet, thermal tolerance in animals adapted to simultaneous warming and acidification is unknown. We experimentally evolved the ubiquitous copepod Acartia tonsa to future combined ocean warming and acidification conditions (OWA approx. 22°C, 2000 µatm CO₂) and then compared its thermal tolerance relative to ambient conditions (AM approx. 18°C, 400 µatm CO₂). The OWA and AM treatments were reciprocally transplanted after 65 generations to assess effects of developmental conditions on thermal tolerance and potential costs of adaptation. Treatments transplanted from OWA to AM conditions were assessed at the F1 and F9 generations following transplant. Adaptation to warming and acidification, paradoxically, reduces both thermal tolerance and phenotypic plasticity. These costs of adaptation to combined warming and acidification may limit future population resilience.     

Vulnerability of stream community composition and function to projected thermal warming and hydrologic change across ecoregions in the western United States

Shifts in biodiversity and ecological processes in stream ecosystems in response to rapid climate change will depend on how numerically and functionally dominant aquatic insect species respond to changes in stream temperature and hydrology. Across 253 minimally perturbed streams in eight ecoregions in the western USA, we modeled the distribution of 88 individual insect taxa in relation to existing combinations of maximum summer temperature, mean annual streamflow, and their interaction. We used a heat map approach along with downscaled general circulation model (GCM) projections of warming and streamflow change to estimate site‐specific extirpation likelihood for each taxon, allowing estimation of whole‐community change in streams across these ecoregions. Conservative climate change projections indicate a 30–40% loss of taxa in warmer, drier ecoregions and 10–20% loss in cooler, wetter ecoregions where taxa are relatively buffered from projected warming and hydrologic change. Differential vulnerability of taxa with key functional foraging roles in processing basal resources suggests that climate change has the potential to modify stream trophic structure and function (e.g., alter rates of detrital decomposition and algal consumption), particularly in warmer and drier ecoregions. We show that streamflow change is equally as important as warming in projected risk to stream community composition and that the relative threat posed by these two fundamental drivers varies across ecoregions according to projected gradients of temperature and hydrologic change. Results also suggest that direct human modification of streams through actions such as water abstraction is likely to further exacerbate loss of taxa and ecosystem alteration, especially in drying climates. Management actions to mitigate climate change impacts on stream ecosystems or to proactively adapt to them will require regional calibration, due to geographic variation in insect sensitivity and in exposure to projected thermal warming and hydrologic change.     

Effects of hypoxia on the thermal physiology of a high-elevation lizard: implications for upslope-shifting species

Montane reptiles are predicted to move to higher elevations in response to climate warming. However, whether upwards-shifting reptiles will be physiologically constrained by hypoxia at higher elevations remains unknown. We investigated the effects of hypoxic conditions on preferred body temperatures (T_pref) and thermal tolerance capacity of a montane lizard (Phrynocephalus vlangalii) from two populations on the Qinghai–Tibet Plateau. Lizards from 2600 m a.s.l. were exposed to O₂ levels mimicking those at 2600 m (control) and 3600 m (hypoxia treatment). Lizards from 3600 m a.s.l. were exposed to O₂ levels mimicking those at 3600 m (control) and 4600 m (hypoxia treatment). The T_pref did not differ between the control and hypoxia treatments in lizards from 2600 m. However, lizards from 3600 m selected lower body temperatures when exposed to the hypoxia treatment mimicking the O₂ level at 4600 m. Additionally, the hypoxia treatment induced lower critical thermal minimum (CT_min) in lizards from both populations, but did not affect the critical thermal maximum (CT_max) in either population. Our results imply that upwards-shifting reptiles may be constrained by hypoxia if a decrease in T_pref reduces thermally dependent fitness traits, despite no observed effect on their heat tolerance.     

Improved heat tolerance in air drives the recurrent evolution of air-breathing

The transition to air-breathing by formerly aquatic species has occurred repeatedly and independently in fish, crabs and other animal phyla, but the proximate drivers of this key innovation remain a long-standing puzzle in evolutionary biology. Most studies attribute the onset of air-breathing to the repeated occurrence of aquatic hypoxia; however, this hypothesis leaves the current geographical distribution of the 300 genera of air-breathing crabs unexplained. Here, we show that their occurrence is mainly related to high environmental temperatures in the tropics. We also demonstrate in an amphibious crab that the reduced cost of oxygen supply in air extends aerobic performance to higher temperatures and thus widens the animal''s thermal niche. These findings suggest that high water temperature as a driver consistently explains the numerous times air-breathing has evolved. The data also indicate a central role for oxygen- and capacity-limited thermal tolerance not only in shaping sensitivity to current climate change but also in underpinning the climate-dependent evolution of animals, in this case the evolution of air-breathing.     

A comparison of water loss and gill areas in two supralittoral amphipods from New Zealand

Total gill area and gill distribution were measured for the sandhopper Talorchestia quoyana (Milne-Edwards) and the beach flea Transorchestia chiliensis (Milne-Edwards). For both species the gill structure and proportional area contributed by individual gills was similar. Gill 6 (G6) was the largest, providing 36% of the gill area in Tal. quoyana and 30% in Tr. chiliensis. The gill area/total dry weight relationships were similar, Y = 1.3 X^0.79 for Tal. quoyana and 1.4 X^0.78 for Tr. chiliensis. Small, medium and large amphipods survived >24 h in aerial conditions close to 100% RH at 15 °C. Rates of water loss in desiccating conditions increased with decreasing RH. Lethal water loss exceeded 30% weight loss for both species. Rate of water loss, (R) mg water loss. mg wet wt tissue. h^–1 exposed to 75% RH for Tr. chiliensis was 0.21, resulting in total mortality within 2 h. Medium Tal. quoyana were the most resistant group surviving 4 h exposure to 75% RH with R = 0.08. Differences in desiccation tolerances of the two amphipods are not explained by body water content, gill area relationships or the larger maximal size of T. quoyana. Results were combined with those from other talitrids to examine the relationship between gill area, water content, desiccation habitat and oxygen consumption in aerial and aquatic conditions. There were no consistent relationship between gill area, O₂ uptake and desiccation resistance. Amphipods show compensatory respiratory adaptation with individuals from all habitats, showing similar rates of oxygen uptake, either in air or in water, whichever was their most usual respiratory medium. Q¹⁰ values close to 2.0 were found in all ecomorphological groups. Sandhoppers, including Tal. quoyana, are best able to survive terrestrial conditions associated with a low humidity environment. It is concluded that the water loss characteristics of Tr. chiliensis limit its distribution on sand beaches to areas of high relative humidities.     

Responses of arthropod populations to warming depend on latitude: evidence from urban heat islands

Biological effects of climate change are expected to vary geographically, with a strong signature of latitude. For ectothermic animals, there is systematic latitudinal variation in the relationship between climate and thermal performance curves, which describe the relationship between temperature and an organism's fitness. Here, we ask whether these documented latitudinal patterns can be generalized to predict arthropod responses to warming across mid‐ and high temperate latitudes, for taxa whose thermal physiology has not been measured. To address this question, we used a novel natural experiment consisting of a series of urban warming gradients at different latitudes. Specifically, we sampled arthropods from a single common street tree species across temperature gradients in four US cities, located from 35.8 to 42.4° latitude. We captured 6746 arthropods in 34 families from 111 sites that varied in summer average temperature by 1.7–3.4 °C within each city. Arthropod responses to warming within each city were characterized as Poisson regression coefficients describing change in abundance per °C for each family. Family responses in the two midlatitude cities were heterogeneous, including significantly negative and positive effects, while those in high‐latitude cities varied no more than expected by chance within each city. We expected high‐latitude taxa to increase in abundance with warming, and they did so in one of the two high‐latitude cities; in the other, Queens (New York City), most taxa declined with warming, perhaps due to habitat loss that was correlated with warming in this city. With the exception of Queens, patterns of family responses to warming were consistent with predictions based on known latitudinal patterns in arthropod physiology relative to regional climate. Heterogeneous responses in midlatitudes may be ecologically disruptive if interacting taxa respond oppositely to warming.     

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.     

Global analysis of thermal tolerance and latitude in ectotherms

A tenet of macroecology is that physiological processes of organisms are linked to large-scale geographical patterns in environmental conditions. Species at higher latitudes experience greater seasonal temperature variation and are consequently predicted to withstand greater temperature extremes. We tested for relationships between breadths of thermal tolerance in ectothermic animals and the latitude of specimen location using all available data, while accounting for habitat, hemisphere, methodological differences and taxonomic affinity. We found that thermal tolerance breadths generally increase with latitude, and do so at a greater rate in the Northern Hemisphere. In terrestrial ectotherms, upper thermal limits vary little while lower thermal limits decrease with latitude. By contrast, marine species display a coherent poleward decrease in both upper and lower thermal limits. Our findings provide comprehensive global support for hypotheses generated from studies at smaller taxonomic subsets and geographical scales. Our results further indicate differences between terrestrial and marine ectotherms in how thermal physiology varies with latitude that may relate to the degree of temperature variability experienced on land and in the ocean.     

Resilience to extreme temperature events: acclimation capacity and body condition of a polymorphic fish in response to thermal stress

Considerable attention has been given to the potential impacts of global climate change on biodiversity. In the present study, we combine understudied themes by examining the ability of a freshwater fish (polymorphic for heat‐sensitivity) to respond to short‐term thermal stress mimicking an extreme temperature event. We simultaneously measured the effect of thermal stress on the body condition of heat‐sensitive and heat‐tolerant forms to evaluate an existing hypothesis regarding the underlying mechanism by which temperature affects the maintenance of genetic variation in this species. Surprisingly, the heat‐sensitive allelic variant increased in body condition equally as much as a heat‐tolerant variant under acute heat stress. More importantly, the heat‐sensitive variant exhibited a significant response to thermal stress, with an upward shift of greater than 2 °C in critical thermal maximum. Our findings suggest a complexity to the relationship between thermal stress and male body condition that may depend on an interaction with other factors such as resource level. Although the evolutionary fate of species with respect to climate change is typically evaluated in terms long‐term adaptive response, short‐term selection events could drastically reduce fitness and reduce evolutionary potential. Our results suggest that heat‐sensitive species may have considerably greater resilience to the short‐term, extreme perturbations to the environment that are expected under climate change. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 504–510.