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.     

Macroevolutionary consequences of profound climate change on niche evolution in marine molluscs over the past three million years

In order to predict the fate of biodiversity in a rapidly changing world, we must first understand how species adapt to new environmental conditions. The long-term evolutionary dynamics of species'' physiological tolerances to differing climatic regimes remain obscure. Here, we unite palaeontological and neontological data to analyse whether species'' environmental tolerances remain stable across 3 Myr of profound climatic changes using 10 phylogenetically, ecologically and developmentally diverse mollusc species from the Atlantic and Gulf Coastal Plains, USA. We additionally investigate whether these species'' upper and lower thermal tolerances are constrained across this interval. We find that these species'' environmental preferences are stable across the duration of their lifetimes, even when faced with significant environmental perturbations. The results suggest that species will respond to current and future warming either by altering distributions to track suitable habitat or, if the pace of change is too rapid, by going extinct. Our findings also support methods that project species'' present-day environmental requirements to future climatic landscapes to assess conservation risks.     

The Role of Temperature in Determining Species' Vulnerability to Ocean Acidification: A Case Study Using Mytilus galloprovincialis

Ocean acidification (OA) is occurring across a backdrop of concurrent environmental changes that may in turn influence species'' responses to OA. Temperature affects many fundamental biological processes and governs key reactions in the seawater carbonate system. It therefore has the potential to offset or exacerbate the effects of OA. While initial studies have examined the combined impacts of warming and OA for a narrow range of climate change scenarios, our mechanistic understanding of the interactive effects of temperature and OA remains limited. Here, we use the blue mussel, Mytilus galloprovincialis, as a model species to test how OA affects the growth of a calcifying invertebrate across a wide range of temperatures encompassing their thermal optimum. Mussels were exposed in the laboratory to a factorial combination of low and high pCO₂ (400 and 1200 µatm CO₂) and temperatures (12, 14, 16, 18, 20, and 24°C) for one month. Results indicate that the effects of OA on shell growth are highly dependent on temperature. Although high CO₂ significantly reduced mussel growth at 14°C, this effect gradually lessened with successive warming to 20°C, illustrating how moderate warming can mediate the effects of OA through temperature''s effects on both physiology and seawater geochemistry. Furthermore, the mussels grew thicker shells in warmer conditions independent of CO₂ treatment. Together, these results highlight the importance of considering the physiological and geochemical interactions between temperature and carbonate chemistry when interpreting species'' vulnerability to OA.     

Evolution of Thermal Response Properties in a Cold-Activated TRP Channel

Animals sense changes in ambient temperature irrespective of whether core body temperature is internally maintained (homeotherms) or subject to environmental variation (poikilotherms). Here we show that a cold-sensitive ion channel, TRPM8, displays dramatically different thermal activation ranges in frogs versus mammals or birds, consistent with variations in these species'' cutaneous and core body temperatures. Thus, somatosensory receptors are not static through evolution, but show functional diversity reflecting the characteristics of an organism''s ecological niche.     

Improved spatial estimates of climate predict patchier species distributions

Aim

Correlative species distribution models (SDMs) combined with spatial layers of climate and species' localities represent a frequently utilized and rapid method for generating spatial estimates of species distributions. However, an SDM is only as accurate as the inputs upon which it is based. Current best‐practice climate layers commonly utilized in SDM (e.g. ANUCLIM) are frequently inaccurate and biased spatially. Here, we statistically downscale 30 years of existing spatial weather estimates against empirical weather data and spatial layers of topography and vegetation to produce highly accurate spatial layers of weather. We proceed to demonstrate the effect of inaccurately quantified spatial data on SDM outcomes.

Location

The Australian Wet Tropics.

Methods

We use Boosted Regression Trees (BRTs) to generate 30 years of spatial estimates of daily maximum and minimum temperature for the study region and aggregate the resultant weather layers into ‘accuCLIM’ climate summaries, comparable with those generated by current best‐practice climate layers. We proceed to generate for seven species of rainforest skink comparable SDMs within species; one model based on ANUCLIM climate estimates and another based on accuCLIM climate estimates.

Results

Boosted Regression Trees weather layers are more accurate with respect to empirically measured temperature, particularly for maximum temperature, when compared to current best‐practice weather layers. ANUCLIM climate layers are least accurate in heavily forested upland regions, frequently over‐predicting empirical mean maximum temperature by as much as 7°. Distributions of the focal species as predicted by accuCLIM were more fragmented and contained less core distributional area.

Conclusion

Combined these results reveal a source of bias in climate‐based SDMs and indicate a solution in the form of statistical downscaling. This technique will allow researchers to produce fine‐grained, ground‐truthed spatial estimates of weather based on existing estimates, which can be aggregated in novel ways, and applied to correlative or process‐based modelling techniques.

     

Projecting marine species range shifts from only temperature can mask climate vulnerability

Climate change is causing range shifts in many marine species, with implications for biodiversity and fisheries. Previous research has mainly focused on how species' ranges will respond to changing ocean temperatures, without accounting for other environmental covariates that could affect future distribution patterns. Here, we integrate habitat suitability modeling approaches, a high‐resolution global climate model projection, and detailed fishery‐independent and ‐dependent faunal datasets from one of the most extensively monitored marine ecosystems—the U.S. Northeast Shelf. We project the responses of 125 species in this region to climate‐driven changes in multiple oceanographic factors (e.g., ocean temperature, salinity, sea surface height) and seabed characteristics (i.e., rugosity and depth). Comparing model outputs based on ocean temperature and seabed characteristics to those that also incorporated salinity and sea surface height (proxies for primary productivity and ocean circulation features), we explored how an emphasis on ocean temperature in projecting species' range shifts can impact assessments of species' climate vulnerability. We found that multifactor habitat suitability models performed better in explaining and predicting species historical distribution patterns than temperature‐based models. We also found that multifactor models provided more concerning assessments of species' future distribution patterns than temperature‐based models, projecting that species' ranges will largely shift northward and become more contracted and fragmented over time. Our results suggest that using ocean temperature as a primary determinant of range shifts can significantly alter projections, masking species' climate vulnerability, and potentially forestalling proactive management.     

Assessing the Congruence of Thermal Niche Estimations Derived from Distribution and Physiological Data. A Test Using Diving Beetles

A basic aim of ecology is to understand the determinants of organismal distribution, the niche concept and species distribution models providing key frameworks to approach the problem. As temperature is one of the most important factors affecting species distribution, the estimation of thermal limits is crucially important for inferring range constraints. It is expectable that thermal physiology data derived from laboratory experiments and species'' occurrences may express different aspects of the species'' niche. However, there is no study systematically testing this prediction in a given taxonomic group while controlling by potential phylogenetic inertia. We estimate the thermal niches of twelve Palaearctic diving beetles species using physiological data derived from experimental analyses in order to examine the extent to which these coincided with those estimated from distribution models based on observed occurrences. We found that thermal niche estimates derived from both approaches lack general congruence, and these results were similar before and after controlling by phylogeny. The congruence between potential distributions obtained from the two different procedures was also explored, and we found again that the percentage of agreement were not very high (∼60%). We confirm that both thermal niche estimates derived from geographical and physiological data are likely to misrepresent the true range of climatic variation that these diving beetles are able to tolerate, and so these procedures could be considered as incomplete but complementary estimations of an inaccessible reality.     

Integrating Sustainable Hunting in Biodiversity Protection in Central Africa: Hot Spots,Weak Spots,and Strong Spots

Wild animals are a primary source of protein (bushmeat) for people living in or near tropical forests. Ideally, the effect of bushmeat harvests should be monitored closely by making regular estimates of offtake rate and size of stock available for exploitation. However, in practice, this is possible in very few situations because it requires both of these aspects to be readily measurable, and even in the best case, entails very considerable time and effort. As alternative, in this study, we use high-resolution, environmental favorability models for terrestrial mammals (N = 165) in Central Africa to map areas of high species richness (hot spots) and hunting susceptibility. Favorability models distinguish localities with environmental conditions that favor the species'' existence from those with detrimental characteristics for its presence. We develop an index for assessing Potential Hunting Sustainability (PHS) of each species based on their ecological characteristics (population density, habitat breadth, rarity and vulnerability), weighted according to restrictive and permissive assumptions of how species'' characteristics are combined. Species are classified into five main hunting sustainability classes using fuzzy logic. Using the accumulated favorability values of all species, and their PHS values, we finally identify weak spots, defined as high diversity regions of especial hunting vulnerability for wildlife, as well as strong spots, defined as high diversity areas of high hunting sustainability potential. Our study uses relatively simple models that employ easily obtainable data of a species'' ecological characteristics to assess the impacts of hunting in tropical regions. It provides information for management by charting the geography of where species are more or less likely to be at risk of extinction from hunting.     

Swimming with Predators and Pesticides: How Environmental Stressors Affect the Thermal Physiology of Tadpoles

To forecast biological responses to changing environments, we need to understand how a species''s physiology varies through space and time and assess how changes in physiological function due to environmental changes may interact with phenotypic changes caused by other types of environmental variation. Amphibian larvae are well known for expressing environmentally induced phenotypes, but relatively little is known about how these responses might interact with changing temperatures and their thermal physiology. To address this question, we studied the thermal physiology of grey treefrog tadpoles (Hyla versicolor) by determining whether exposures to predator cues and an herbicide (Roundup) can alter their critical maximum temperature (CT_max) and their swimming speed across a range of temperatures, which provides estimates of optimal temperature (T_opt) for swimming speed and the shape of the thermal performance curve (TPC). We discovered that predator cues induced a 0.4°C higher CT_max value, whereas the herbicide had no effect. Tadpoles exposed to predator cues or the herbicide swam faster than control tadpoles and the increase in burst speed was higher near T_opt. In regard to the shape of the TPC, exposure to predator cues increased T_opt by 1.5°C, while exposure to the herbicide marginally lowered T_opt by 0.4°C. Combining predator cues and the herbicide produced an intermediate T_opt that was 0.5°C higher than the control. To our knowledge this is the first study to demonstrate a predator altering the thermal physiology of amphibian larvae (prey) by increasing CT_max, increasing the optimum temperature, and producing changes in the thermal performance curves. Furthermore, these plastic responses of CT_max and TPC to different inducing environments should be considered when forecasting biological responses to global warming.     

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.     

A Mechanistic Niche Model for Measuring Species' Distributional Responses to Seasonal Temperature Gradients

Niche theory is central to understanding how species respond geographically to climate change. It defines a species'' realized niche in a biological community, its fundamental niche as determined by physiology, and its potential niche—the fundamental niche in a given environment or geographic space. However, most predictions of the effects of climate change on species'' distributions are limited to correlative models of the realized niche, which assume that species are in distributional equilibrium with respect to the variables or gradients included in the model. Here, I present a mechanistic niche model that measures species'' responses to major seasonal temperature gradients that interact with the physiology of the organism. I then use lethal physiological temperatures to parameterize the model for bird species in North and South America and show that most focal bird species are not in direct physiological equilibrium with the gradients. Results also show that most focal bird species possess broad thermal tolerances encompassing novel climates that could become available with climate change. I conclude with discussion of how mechanistic niche models may be used to (i) gain insights into the processes that cause species to respond to climate change and (ii) build more accurate correlative distribution models in birds and other species.     

A pantropical analysis of the impacts of forest degradation and conversion on local temperature

Temperature is a core component of a species' fundamental niche. At the fine scale over which most organisms experience climate (mm to ha), temperature depends upon the amount of radiation reaching the Earth's surface, which is principally governed by vegetation. Tropical regions have undergone widespread and extreme changes to vegetation, particularly through the degradation and conversion of rainforests. As most terrestrial biodiversity is in the tropics, and many of these species possess narrow thermal limits, it is important to identify local thermal impacts of rainforest degradation and conversion. We collected pantropical, site‐level (<1 ha) temperature data from the literature to quantify impacts of land‐use change on local temperatures, and to examine whether this relationship differed aboveground relative to belowground and between wet and dry seasons. We found that local temperature in our sample sites was higher than primary forest in all human‐impacted land‐use types (N = 113,894 daytime temperature measurements from 25 studies). Warming was pronounced following conversion of forest to agricultural land (minimum +1.6°C, maximum +13.6°C), but minimal and nonsignificant when compared to forest degradation (e.g., by selective logging; minimum +1°C, maximum +1.1°C). The effect was buffered belowground (minimum buffering 0°C, maximum buffering 11.4°C), whereas seasonality had minimal impact (maximum buffering 1.9°C). We conclude that forest‐dependent species that persist following conversion of rainforest have experienced substantial local warming. Deforestation pushes these species closer to their thermal limits, making it more likely that compounding effects of future perturbations, such as severe droughts and global warming, will exceed species' tolerances. By contrast, degraded forests and belowground habitats may provide important refugia for thermally restricted species in landscapes dominated by agricultural land.     

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.     

Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology

The environmental conditions in the ocean have long been considered relatively more stable through time compared to the conditions on land. Advances in sensing technologies, however, are increasingly revealing substantial fluctuations in abiotic factors over ecologically and evolutionarily relevant timescales in the ocean, leading to a growing recognition of the dynamism of the marine environment as well as new questions about how this dynamism may influence species' vulnerability to global environmental change. In some instances, the diurnal or seasonal variability in major environmental change drivers, such as temperature, pH and seawater carbonate chemistry, and dissolved oxygen, can exceed the changes expected with continued anthropogenic global change. While ocean global change biologists have begun to experimentally test how variability in environmental conditions mediates species' responses to changes in the mean, the extensive literature on species' adaptations to temporal variability in their environment and the implications of this variability for their evolutionary responses has not been well integrated into the field. Here, we review the physiological mechanisms underlying species' responses to changes in temperature, pCO₂/pH (and other carbonate parameters), and dissolved oxygen, and discuss what is known about behavioral, plastic, and evolutionary strategies for dealing with variable environments. In addition, we discuss how exposure to variability may influence species' responses to changes in the mean conditions and highlight key research needs for ocean global change biology.     

Predicting fundamental and realized distributions based on thermal niche: A case study of a freshwater turtle

Species distribution models (SDM) have been broadly used in ecology to address theoretical and practical problems. Currently, there are two main approaches to generate SDMs: (i) correlative, which is based on species occurrences and environmental predictor layers and (ii) process-based models, which are constructed based on species' functional traits and physiological tolerances. The distributions estimated by each approach are based on different components of species niche. Predictions of correlative models approach species realized niches, while predictions of process-based are more akin to species fundamental niche. Here, we integrated the predictions of fundamental and realized distributions of the freshwater turtle Trachemys dorbigni. Fundamental distribution was estimated using data of T. dorbigni's egg incubation temperature, and realized distribution was estimated using species occurrence records. Both types of distributions were estimated using the same regression approaches (logistic regression and support vector machines), both considering macroclimatic and microclimatic temperatures. The realized distribution of T. dorbigni was generally nested in its fundamental distribution reinforcing theoretical assumptions that the species' realized niche is a subset of its fundamental niche. Both modelling algorithms produced similar results but microtemperature generated better results than macrotemperature for the incubation model. Finally, our results reinforce the conclusion that species realized distributions are constrained by other factors other than just thermal tolerances.     

A heterogeneous thermal environment enables remarkable behavioral thermoregulation in Uta stansburiana

Ectotherms can attain preferred body temperatures by selecting specific temperature microhabitats within a varied thermal environment. The side‐blotched lizard, Uta stansburiana may employ microhabitat selection to thermoregulate behaviorally. It is unknown to what degree habitat structural complexity provides thermal microhabitats for thermoregulation. Thermal microhabitat structure, lizard temperature, and substrate preference were simultaneously evaluated using thermal imaging. A broad range of microhabitat temperatures was available (mean range of 11°C within 1–2 m²) while mean lizard temperature was between 36°C and 38°C. Lizards selected sites that differed significantly from the mean environmental temperature, indicating behavioral thermoregulation, and maintained a temperature significantly above that of their perch (mean difference of 2.6°C). Uta's thermoregulatory potential within a complex thermal microhabitat structure suggests that a warming trend may prove advantageous, rather than detrimental for this population.     

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

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

Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability

Although theory suggests geographic variation in species' performance is determined by multiple niche parameters, little consideration has been given to the spatial structure of interacting stressors that may shape local and regional vulnerability to global change. Here, we use spatially explicit mosaics of carbonate chemistry, food availability and temperature spanning 1280 km of coastline to test whether persistent, overlapping environmental mosaics mediate the growth and predation vulnerability of a critical foundation species, the mussel Mytilus californianus. We find growth was highest and predation vulnerability was lowest in dynamic environments with frequent exposure to low pH seawater and consistent food. In contrast, growth was lowest and predation vulnerability highest when exposure to low pH seawater was decoupled from high food availability, or in exceptionally warm locations. These results illustrate how interactions among multiple drivers can cause unexpected, yet persistent geographic mosaics of species performance, interactions and vulnerability to environmental change.     

Variable choice affects estimations of vulnerability to climate change

For practical reasons, assessments of species' vulnerability to rising temperatures are often limited to measuring responses to a single ecological response variable, but this could result in an underestimation of vulnerability. Using the Cape Rockjumper Chaetops frenatus (‘Rockjumper’) we examined the thermal risk to nestling Rockjumpers for sublethal (i.e. reduced nestling mass gain) and lethal (i.e. increased nest predation) consequences of sustained hot weather under both current and predicted future climatic conditions (RCP 8.5). We used a direct approach to examine these risks, first as independent ecological responses and then as combined risk driven by both response variables (mass gain and predation risk). This study revealed that the inclusion of multiple climate-related responses affected the predicted vulnerability to climate change. Further, our analyses showed that increased vulnerability to climate change will vary within the Rockjumper's habitat. Our results demonstrate that the variability in predicted thermal risk depends on which response variable was used, with implications for how and where conservation practitioners direct their already limited resources.