Ecological and physiological thermal niches to understand distribution of Chagas disease vectors in Latin America

In order to assess how triatomines (Hemiptera, Reduviidae), Chagas disease vectors, are distributed through Latin America, we analysed the relationship between the ecological niche and the limits of the physiological thermal niche in seven species of triatomines. We combined two methodological approaches: species distribution models, and physiological tolerances. First, we modelled the ecological niche and identified the most important abiotic factor for their distribution. Then, thermal tolerance limits were analysed by measuring maximum and minimum critical temperatures, upper lethal temperature, and ‘chill‐coma recovery time’. Finally, we used phylogenetic independent contrasts to analyse the link between limiting factors and the thermal tolerance range for the assessment of ecological hypotheses that provide a different outlook for the geo‐epidemiology of Chagas disease. In triatomines, thermo‐tolerance range increases with increasing latitude mainly due to better cold tolerances, suggesting an effect of thermal selection. In turn, physiological analyses show that species reaching southernmost areas have a higher thermo‐tolerance than those with tropical distributions, denoting that thermo‐tolerance is limiting the southern distribution. Understanding the latitudinal range along its physiological limits of disease vectors may prove useful to test ecological hypotheses and improve strategies and efficiency of vector control at the local and regional levels.     

Upper temperature limits of tropical marine ectotherms: global warming implications

Animal physiology, ecology and evolution are affected by temperature and it is expected that community structure will be strongly influenced by global warming. This is particularly relevant in the tropics, where organisms are already living close to their upper temperature limits and hence are highly vulnerable to rising temperature. Here we present data on upper temperature limits of 34 tropical marine ectotherm species from seven phyla living in intertidal and subtidal habitats. Short term thermal tolerances and vertical distributions were correlated, i.e., upper shore animals have higher thermal tolerance than lower shore and subtidal animals; however, animals, despite their respective tidal height, were susceptible to the same temperature in the long term. When temperatures were raised by 1°C hour(-1), the upper lethal temperature range of intertidal ectotherms was 41-52°C, but this range was narrower and reduced to 37-41°C in subtidal animals. The rate of temperature change, however, affected intertidal and subtidal animals differently. In chronic heating experiments when temperature was raised weekly or monthly instead of every hour, upper temperature limits of subtidal species decreased from 40°C to 35.4°C, while the decrease was more than 10°C in high shore organisms. Hence in the long term, activity and survival of tropical marine organisms could be compromised just 2-3°C above present seawater temperatures. Differences between animals from environments that experience different levels of temperature variability suggest that the physiological mechanisms underlying thermal sensitivity may vary at different rates of warming.     

Critical thermal limits depend on methodological context

A full-factorial study of the effects of rates of temperature change and start temperatures was undertaken for both upper and lower critical thermal limits (CTLs) using the tsetse fly, Glossina pallidipes. Results show that rates of temperature change and start temperatures have highly significant effects on CTLs, although the duration of the experiment also has a major effect. Contrary to a widely held expectation, slower rates of temperature change (i.e. longer experimental duration) resulted in poorer thermal tolerance at both high and low temperatures. Thus, across treatments, a negative relationship existed between duration and upper CTL while a positive relationship existed between duration and lower CTL. Most importantly, for predicting tsetse distribution, G. pallidipes suffer loss of function at less severe temperatures under the most ecologically relevant experimental conditions for upper (0.06 degrees C min(-1); 35 degrees C start temperature) and lower CTL (0.06 degrees C min(-1); 24 degrees C start temperature). This suggests that the functional thermal range of G. pallidipes in the wild may be much narrower than previously suspected, approximately 20-40 degrees C, and highlights their sensitivity to even moderate temperature variation. These effects are explained by limited plasticity of CTLs in this species over short time scales. The results of the present study have broad implications for understanding temperature tolerance in these and other terrestrial arthropods.     

An alternative explanation for global trends in thermal tolerance

Ectotherms from higher latitudes can generally perform over broader temperature ranges than tropical ectotherms. This pattern is thought to reflect trends in temperature variability: tropical ectotherms evolve to be ‘thermal specialists’ because their environment is thermally stable. However, the tropics are also hotter, and most physiological rates increase exponentially with temperature. Using a dataset spanning diverse ectotherms, we show that the temperature ranges ectotherms tolerate (the difference between lower and upper critical temperatures, and between optimum and upper critical temperatures) generally represents the same range of equivalent biological rates (e.g. metabolism) for cool‐ and warm‐adapted species, and independent of latitude or elevation. This suggests that geographical trends in temperature variability may not be the ultimate mechanism underlying latitudinal and elevational trends in thermal tolerance. Rather, we propose that tropical ectotherms can perform over a narrower range of temperatures than species from higher latitudes because the tropics are hotter.     

Oxygen limits heat tolerance and drives heat hardening in the aquatic nymphs of the gill breathing damselfly Calopteryx virgo (Linnaeus, 1758)

Thermal limits in ectotherms may arise through a mismatch between O₂ supply and demand. At higher temperatures, the ability of their cardiac and ventilatory activities to supply O₂ becomes insufficient to meet their elevated O₂ demand. Consequently, higher levels of O₂ in the environment are predicted to enhance heat tolerance, while reductions in O₂ are expected to reduce thermal limits. Here, we extend previous research on thermal limits and oxygen limitation in aquatic insect larvae and report critical upper temperatures in nymphs of the damselfly Calopteryx virgo (Linnaeus, 1758) exposed to different levels of O₂. In addition, we explore the potential for a mechanistic link between O₂ conditions and thermal plasticity by exposing nymphs to two consecutive extreme heat events, using different levels of O₂ in the second exposure. As predicted, hypoxia severely lowered critical temperatures. However, thermal tolerance was not improved under hyperoxia. Damselfly nymphs may be precluded to take advantage of hyperoxia if O₂ uptake and delivery is controlled locally near the caudal gills where most of the gas exchange occurs. The same asymmetrical effects of hypoxia and hyperoxia on heat tolerance in terrestrial insects could be similarly explained if tracheal opening and/or ventilation are not centrally regulated. Prior exposure to hypoxia enhanced critical thermal maxima in subsequent heat exposures and hyperoxia negated this hardening effect, indicating potential for oxygen-driven heat hardening in these aquatic insects. Our study provides broad confirmation for oxygen limitation as a key mechanism setting upper thermal limits, pointing to a vital role for heat shock proteins in reducing O₂ requirements by slowing down rates of protein denaturation.     

Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits?

The potential of populations to evolve in response to ongoing climate change is partly conditioned by the presence of heritable genetic variation in relevant physiological traits. Recent research suggests that Drosophila melanogaster exhibits negligible heritability, hence little evolutionary potential in heat tolerance when measured under slow heating rates that presumably mimic conditions in nature. Here, we study the effects of directional selection for increased heat tolerance using Drosophila as a model system. We combine a physiological model to simulate thermal tolerance assays with multilocus models for quantitative traits. Our simulations show that, whereas the evolutionary response of the genetically determined upper thermal limit (CTmax) is independent of methodological context, the response in knockdown temperatures varies with measurement protocol and is substantially (up to 50%) lower than for CTmax. Realized heritabilities of knockdown temperature may grossly underestimate the true heritability of CTmax. For instance, assuming that the true heritability of CTmax in the base population is h² = 0.25, realized heritabilities of knockdown temperature are around 0.08–0.16 depending on heating rate. These effects are higher in slow heating assays, suggesting that flawed methodology might explain the apparently limited evolutionary potential of cosmopolitan D. melanogaster.     

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.     

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.     

Divergence of thermal physiological traits in terrestrial breeding frogs along a tropical elevational gradient

Critical thermal limits are thought to be correlated with the elevational distribution of species living in tropical montane regions, but with upper limits being relatively invariant compared to lower limits. To test this hypothesis, we examined the variation of thermal physiological traits in a group of terrestrial breeding frogs (Craugastoridae) distributed along a tropical elevational gradient. We measured the critical thermal maximum (CT_max; n = 22 species) and critical thermal minimum (CT_min; n = 14 species) of frogs captured between the Amazon floodplain (250 m asl) and the high Andes (3,800 m asl). After inferring a multilocus species tree, we conducted a phylogenetically informed test of whether body size, body mass, and elevation contributed to the observed variation in CT_max and CT_min along the gradient. We also tested whether CT_max and CT_min exhibit different rates of change given that critical thermal limits (and their plasticity) may have evolved differently in response to different temperature constraints along the gradient. Variation of critical thermal traits was significantly correlated with species’ elevational midpoint, their maximum and minimum elevations, as well as the maximum air temperature and the maximum operative temperature as measured across this gradient. Both thermal limits showed substantial variation, but CT_min exhibited relatively faster rates of change than CT_max, as observed in other taxa. Nonetheless, our findings call for caution in assuming inflexibility of upper thermal limits and underscore the value of collecting additional empirical data on species’ thermal physiology across elevational gradients.     

Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts

For tsetse (Glossina spp.), the vectors of human and animal trypanosomiases, the physiological mechanisms linking variation in population dynamics with changing weather conditions have not been well established. Here, we investigate high- and low-temperature tolerance in terms of activity limits and survival in a natural population of adult Glossina pallidipes from eastern Zambia. Due to increased interest in chilling flies for handling and aerial dispersal in sterile insect technique control and eradication programmes, we also provide further detailed investigation of low-temperature responses. In wild-caught G. pallidipes, the probability of survival for 50% of the population at low-temperatures was at 3.7, 8.9 and 9.6 degrees C (95% CIs: +/-1.5 degrees C) for 1, 2 and 3 h treatments, respectively. At high temperatures, it was estimated that treatments at 37.9, 36.2 and 35.6 degrees C (95% CIs: +/-0.5 degrees C) would yield 50% population survival for 1, 2 and 3 h, respectively. Significant effects of time and temperature were detected at both temperature extremes (GLZ, p<0.05 in all cases) although a time-temperature interaction was only detected at high temperatures (p<0.0001). We synthesized data from four other Kenyan populations and found that upper critical thermal limits showed little variation among populations and laboratory treatments (range: 43.9-45.0 degrees C; 0.25 degrees C/min heating rate), although reduction to more ecologically relevant heating rates (0.06 degrees C/min) reduce these values significantly from approximately 44.4 to 40.6 degrees C, thereby providing a causal explanation for why tsetse distribution may be high-temperature limited. By contrast, low-temperature limits showed substantial variation among populations and acclimation treatments (range: 4.5-13.8 degrees C; 0.25 degrees C/min), indicating high levels of inter-population variability. Ecologically relevant cooling rates (0.06 degrees C/min) suggest tsetses are likely to experience chill coma temperatures under natural conditions (approximately 20-21 degrees C). The results from acute hardening experiments in the Zambian population demonstrate limited ability to improve low-temperature tolerance over short (hourly) timescales after non-lethal pre-treatments. In flies which survived chilling, recovery times were non-linear with plateaus between 2-6 and 8-12 degrees C. Survival times ranged between 4 and 36 h and did not vary between flies which had undergone chill coma by comparison with flies which had not, even after factoring body condition into the analyses (p>0.5 in all cases). However, flies with low chill coma values had the highest body water and fat content, indicating that when energy reserves are depleted, low-temperature tolerance may be compromised. Overall, these results suggest that physiological mechanisms may provide insight into tsetse population dynamics, hence distribution and abundance, and support a general prediction for reduced geographic distribution under future climate warming scenarios.     

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.     

Critical thermal maxima of early life stages of three tropical fishes: Effects of rearing temperature and experimental heating rate

Marine ectotherms are often sensitive to thermal stress, and certain life stages can be particularly vulnerable (e.g., larvae or spawners). In this study, we investigated the critical thermal maxima (CT_max) of larval and early juvenile life stages of three tropical marine fishes (Acanthochromis polyacanthus, Amphiprion melanopus, and Lates calcarifer). We tested for potential effects of developmental acclimation, life stage, and experimental heating rates, and we measured metabolic enzyme activities from aerobic (citrate synthase, CS) and anaerobic pathways (lactate dehydrogenase, LDH). A slightly elevated rearing temperature neither influenced CT_max nor CS activity, which otherwise could have indicated thermal acclimation. However, we found CT_max to either remain stable (Acanthrochromis polyacanthus) or increase with body mass during early ontogeny (Amphiprion melanopus and Lates calcarifer). In all three species, faster heating rates lead to higher CT_max. Acute temperature stress did not change CS or LDH activities, suggesting that overall aerobic and anaerobic metabolism remained stable. Lates calcarifer, a catadromous species that migrates from oceanic to riverine habitats upon metamorphosis, had higher CT_max than the two coral reef fish species. We highlight that, for obtaining conservative estimates of a fish species’ upper thermal limits, several developmental stages and body mass ranges should be examined. Moreover, upper thermal limits should be assessed using standardized heating rates. This will not only benefit comparative approaches but also aid in assessing geographic (re-) distributions and climate change sensitivity of marine fishes.     

A comparative analysis of the upper thermal tolerance limits of eastern Pacific porcelain crabs, genus Petrolisthes: influences of latitude, vertical zonation, acclimation, and phylogeny

Marine intertidal organisms are subjected to a variety of abiotic stresses, including aerial exposure and wide ranges of temperature. Intertidal species generally have higher thermal tolerance limits than do subtidal species, and tropical species have higher thermal tolerance limits than do temperate species. The adaptive significance of upper thermal tolerance limits of intertidal organisms, however, has not been examined within a comparative context. Here, we present a comparative analysis of the adaptive significance of upper thermal tolerance limits in 20 congeneric species of porcelain crabs, genus Petrolisthes, from intertidal and subtidal habitats throughout the eastern Pacific. Upper thermal tolerance limits are positively correlated with surface water temperatures and with maximal microhabitat temperatures. Analysis of phylogenetically independent contrasts (from a phylogenetic tree on the basis of the 16s rDNA gene sequence) suggests that upper thermal tolerance limits have evolved in response to maximal microhabitat temperatures. Upper thermal tolerance limits increased during thermal acclimation at elevated temperatures, the amount of increase being greater for subtidal than for intertidal species. This result suggests that the upper thermal tolerance limits of some intertidal species may be near current habitat temperature maxima, and global warming thus may affect the distribution limits of intertidal species to a greater extent than for subtidal species.     

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.     

Acclimation effects on critical and lethal thermal limits of workers of the Argentine ant, Linepithema humile

For the Argentine ant Linepithema humile, bioclimatic models often predict narrower optimal temperature ranges than those suggested by behavioural and physiological studies. Although water balance characteristics of workers of this species have been thoroughly studied, gaps exist in current understanding of its thermal limits. We investigated critical thermal minima and maxima and upper and lower lethal limits following acclimation to four temperatures (15, 20, 25, 30 degrees C; 12L:12D photoperiod) in adult workers of the Argentine ant, L. humile, collected from Stellenbosch, South Africa. At an ecologically relevant rate of temperature change of 0.05 degrees Cmin(-1), CTMax varied between 38 and 40 degrees C, and CTMin varied between 0 and 0.8 degrees C. In both cases the response to acclimation was weak. A significant time by exposure temperature interaction was found for upper and lower lethal limits, with a more pronounced effect of acclimation at longer exposure durations. Upper lethal limits varied between 37 and 44 degrees C, whilst lower lethal limits varied between -4 and -10.5 degrees C, with an acclimation effect more pronounced for upper than lower lethal limits. A thermal envelope for workers of the Argentine ant is provided, demonstrating that upper thermal limits do likely contribute to distributional limits, but that lower lethal limits and limits to activity likely do not, or at least for workers who are not exposed simultaneously to the demands of load carriage and successful foraging behaviour.     

Temperature and water relations in desert bees

1. 1. Desert bees do not show significant differences in most thermal parameters; mean endothermic warm-up rates are similar to those of temperate species, with no special cooling mechanisms, and normal upper critical temperatures (unlike desert ants and beetles). Thermoregulatory abilities may however be improved.

2. 2. They show the whole range of possible water balance problems; small species are acutely water-stressed when foraging, but large bees suffer from excessive generation of metabolic water in flight.

3. 3. Activity patterns are therefore either matinal, crepuscular or bimodal; essentially desert bees avoid heat and adapt to cold desert dawns and dusks. Desert plants must be coevolved to offer appropriate rewards and match the physiological constraints on their pollinators.

4. 4. Endothermy in bees may have evolved primarily in arid zones, and served as a pre-adaptation for subsequent invasion of cool temperate biomes.

     

虎纹蛙选择体温和热耐受性在个体发育过程中的变化

体温是影响变温动物表现的最重要生理学变量。检测了国家二级保护动物虎纹蛙的雌性亚成体、雄性亚成体、幼体和蝌蚪这4个发育阶段的选择体温和热耐受性。单因子方差分析表明,虎纹蛙选择体温、耐受低温、耐受高温和温度耐受范围的组间差异均显著,幼体的选择体温(24.13℃)显著低于雌性亚成体(28.06℃)、雄性亚成体(29.27℃)和蝌蚪(28.23℃),雌性亚成体、雄性亚成体和蝌蚪之间差异不显著;幼体的耐受低温(13.85℃)显著高于雌性亚成体(11.27℃)、雄性亚成体(10.84℃)和蝌蚪(10.74℃),雌性亚成体、雄性亚成体和蝌蚪之间差异不显著;幼体具有显著低的耐受高温(35.48℃)、蝌蚪具有显著高的耐受高温(43.31℃),雌性亚成体(39.55℃)和雄性亚成体(39.02℃)的耐受高温差异不显著;幼体(21.62℃)具有显著小的温度耐受范围、蝌蚪(32.58℃)具有显著大的温度耐受范围,雌性亚成体(28.28℃)和雄性亚成体(28.18℃)的温度耐受范围差异不显著。虎纹蛙幼体和亚成体体温和水温之间在降温速度和升温速度的相关关系均显著。用回归剩余值去除水温变化速度对体温变化的影响,双因子方差分析(降温和升温速度为重复检验设置)表明,幼体的体温变化速度显著大于亚成体,两性亚成体间差异不显著;温度变化类型(降温和升温)和两因子的交互作用对体温变化的影响不显著。基本热生态位分离和体温调节能力的发育限制是形成上述现象的最可能的原因。     

Plastic collective endothermy in a complex animal society (army ant bivouacs: Eciton burchellii parvispinum)

Endothermic animals do not always have a single adaptive internal temperature; some species exhibit plastic homeostasis, adaptively allowing body temperature to drop when thermoregulatory costs are high. Like large‐bodied endotherms, some animal societies exhibit collective thermal homeostasis. We tested for plasticity of thermoregulation in the self‐assembled temporary nests (bivouacs) of army ants. We measured core bivouac temperatures under a range of environmental conditions and at different colony developmental (larval vs pupal brood) stages. Contrary to previous assertions, bivouacs were not perfect thermoregulators in all developmental stages. Instead, bivouacs functioned as superorganismal facultative endotherms, using a combination of site choice and context‐dependent metabolic heating to adjust core temperatures across an elevational cline in ambient temperature. When ambient temperature was low, the magnitude of metabolic heating was dependent on colony developmental stage: pupal bivouacs were warmer than larval bivouacs. At cooler high elevations, bivouacs functioned like some endothermic animals that intermittently lower their body temperatures to conserve energy. Bivouacs potentially conserved energy by investing less metabolic heating in larval brood because the high costs of impaired worker development may require more stringent thermoregulation of pupae. Our data also suggest that site choice played an important role in bivouac cooling under high ambient temperatures at low elevations. Climate warming may expand upper elevational range limits of Eciton burchellii parvispinum, while reducing the availability of cool and moist bivouac sites at lower elevations, potentially leading to future low‐elevation range contraction.     

Integrating metabolic performance,thermal tolerance,and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming

Predicting species vulnerability to global warming requires a comprehensive, mechanistic understanding of sublethal and lethal thermal tolerances. To date, however, most studies investigating species physiological responses to increasing temperature have focused on the underlying physiological traits of either acute or chronic tolerance in isolation. Here we propose an integrative, synthetic approach including the investigation of multiple physiological traits (metabolic performance and thermal tolerance), and their plasticity, to provide more accurate and balanced predictions on species and assemblage vulnerability to both acute and chronic effects of global warming. We applied this approach to more accurately elucidate relative species vulnerability to warming within an assemblage of six caridean prawns occurring in the same geographic, hence macroclimatic, region, but living in different thermal habitats. Prawns were exposed to four incubation temperatures (10, 15, 20 and 25 °C) for 7 days, their metabolic rates and upper thermal limits were measured, and plasticity was calculated according to the concept of Reaction Norms, as well as Q₁₀ for metabolism. Compared to species occupying narrower/more stable thermal niches, species inhabiting broader/more variable thermal environments (including the invasive Palaemon macrodactylus) are likely to be less vulnerable to extreme acute thermal events as a result of their higher upper thermal limits. Nevertheless, they may be at greater risk from chronic exposure to warming due to the greater metabolic costs they incur. Indeed, a trade‐off between acute and chronic tolerance was apparent in the assemblage investigated. However, the invasive species P. macrodactylus represents an exception to this pattern, showing elevated thermal limits and plasticity of these limits, as well as a high metabolic control. In general, integrating multiple proxies for species physiological acute and chronic responses to increasing temperature helps providing more accurate predictions on species vulnerability to warming.     

Microhabitats reduce animal's exposure to climate extremes

Extreme weather events, such as unusually hot or dry conditions, can cause death by exceeding physiological limits, and so cause loss of population. Survival will depend on whether or not susceptible organisms can find refuges that buffer extreme conditions. Microhabitats offer different microclimates to those found within the wider ecosystem, but do these microhabitats effectively buffer extreme climate events relative to the physiological requirements of the animals that frequent them? We collected temperature data from four common microhabitats (soil, tree holes, epiphytes, and vegetation) located from the ground to canopy in primary rainforests in the Philippines. Ambient temperatures were monitored from outside of each microhabitat and from the upper forest canopy, which represent our macrohabitat controls. We measured the critical thermal maxima (CT_max) of frog and lizard species, which are thermally sensitive and inhabit our microhabitats. Microhabitats reduced mean temperature by 1–2 °C and reduced the duration of extreme temperature exposure by 14–31 times. Microhabitat temperatures were below the CT_max of inhabitant frogs and lizards, whereas macrohabitats consistently contained lethal temperatures. Microhabitat temperatures increased by 0.11–0.66 °C for every 1 °C increase in macrohabitat temperature, and this nonuniformity in temperature change influenced our forecasts of vulnerability for animal communities under climate change. Assuming uniform increases of 6 °C, microhabitats decreased the vulnerability of communities by up to 32‐fold, whereas under nonuniform increases of 0.66 to 3.96 °C, microhabitats decreased the vulnerability of communities by up to 108‐fold. Microhabitats have extraordinary potential to buffer climate and likely reduce mortality during extreme climate events. These results suggest that predicted changes in distribution due to mortality and habitat shifts that are derived from macroclimatic samples and that assume uniform changes in microclimates relative to macroclimates may be overly pessimistic. Nevertheless, even nonuniform temperature increases within buffered microhabitats would still threaten frogs and lizards.