Research on the thermal ecology and physiology of free-living organisms is accelerating as scientists and managers recognize the urgency of the global biodiversity crisis brought on by climate change. As ectotherms, temperature fundamentally affects most aspects of the lives of amphibians and reptiles, making them excellent models for studying how animals are impacted by changing temperatures. As research on this group of organisms accelerates, it is essential to maintain consistent and optimal methodology so that results can be compared across groups and over time. This review addresses the utility of reptiles and amphibians as model organisms for thermal studies by reviewing the best practices for research on their thermal ecology and physiology, and by highlighting key studies that have advanced the field with new and improved methods. We end by presenting several areas where reptiles and amphibians show great promise for further advancing our understanding of how temperature relations between organisms and their environments are impacted by global climate change.

The thermal ecology and physiology of reptiles and amphibians: A user's guide.

Extinction rates are predicted to rise exponentially under climate warming, but many of these predictions ignore physiological and behavioral plasticity that might buffer species from extinction. We evaluated the potential for physiological acclimatization and behavioral avoidance of poor climatic conditions to lower extinction risk under climate change in the global hotspot of salamander diversity, a region currently predicted to lose most of the salamander habitat due to warming. Our approach integrated experimental physiology and behavior into a mechanistic species distribution model to predict extinction risk based on an individual’s capacity to maintain energy balance with and without plasticity. We assessed the sensitivity of extinction risk to body size, behavioral strategies, limitations on energy intake, and physiological acclimatization of water loss and metabolic rate. The field and laboratory experiments indicated that salamanders readily acclimatize water loss rates and metabolic rates in ways that could maintain positive energy balance. Projections with plasticity reduced extinction risk by 72% under climate warming, especially in the core of their range. Further analyses revealed that juveniles might experience the greatest physiological stress under climate warming, but we identified specific physiological adaptations or plastic responses that could minimize the lethal physiological stress imposed on juveniles. We conclude that incorporating plasticity fundamentally alters ecological predictions under climate change by reducing extinction risk in the hotspot of salamander diversity.

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Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity

Mechanistic forecasts of how species will respond to climate change are highly desired but difficult to achieve. Because processes at different scales are explicit in such models, careful assessments of their predictive abilities can provide valuable insights that will be relevant to functionally similar species. However, there are surprisingly few comprehensive field tests of mechanistic niche models in the literature. We applied a general, thermodynamically grounded modeling framework to determine the fundamental niche of an extremely well-studied herbivorous ectotherm, the sleepy lizard Tiliqua rugosa. We then compared the model predictions with detailed long-term field observations that included sub-hourly data on microclimate, activity levels, home ranges, and body temperatures as well as annual to decadal patterns of body condition and growth. Body temperature predictions inferred from gridded climatic data were within 10% of empirically observed values and explained >70% of observed daytime activity patterns across all lizards. However, some periods of activity restriction were explained by predicted desiccation level rather than by temperature, and metabolically driven activity requirements were much lower than potential activity time. Decadal trajectories of field growth and body condition could also be explained to within 10% of observed values, with the variance in trajectories being attributable to whether individuals had access to permanent water. Continent-wide applications of the model partly captured the inland distribution limit, but only after accounting for water limitations. Predicted changes in habitat suitability under six climate change scenarios were generally positive within the species’ current range, but varied strongly with predicted rainfall. Temperature is regarded as the major factor that will restrict the distribution and abundance of lizards and other terrestrial ectotherms under climate change. Yet our findings show how water can be more important than temperature in constraining the activity, habitat requirements, and distribution limits of terrestrial ectotherms. Our results demonstrate the feasibility of first-principles computation of the climatic limits on terrestrial animals from gridded environmental data, providing a coherent picture for how species will respond to climate change at different scales of space and time.

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Field tests of a general ectotherm niche model show how water can limit lizard activity and distribution

s were screened for relevance of physiological data on each species’ response to hypoxia or high elevations. Data base Biosis Citation Index, Zoological Record, Medline Terms included in Boolean search TS = ((\"bar-headed goose\" OR \"anser indicus\") And (\"highaltitude\" OR \"hypox*\" OR \"high elevation\")) TS = ((\"canada goose\" OR \"branta canadensis\") And (\"highaltitude\" OR \"hypox*\" OR \"high elevation\")) TS = ((\"evening grosbeak\" OR \"Coccothraustes vespertinus\") And (\"highaltitude\" OR \"hypox*\" OR \"high elevation\")) 0 Selection Criteria 1. Must be a published article. No meeting abstracts or presentations. 2. Must include the species in question as one of the primary species being reported on. Reporting on another species and simple comparisons (e.g. hemoglobin structure of a species not of interest compared to species of interest) do not meet the requirements. 3. Be associated with high elevation/altitude or hypoxia research. 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Counterpoint: high altitude is not for the birds! J Appl Physiology Bethesda Md 1985 111: 1515–8. McCracken, K. G. et al. 2010. Phylogenetic and structural analysis of the HbA (alphaA/betaA) and HbD (alphaD/betaA) hemoglobin genes in two high-altitude waterfowl from the Himalayas and the Andes: Bar-headed goose (Anser indicus) and Andean goose (Chloephaga melanoptera). Mol Phylogenet Evol 56: 649–58. Meir, J. U. and Milsom, W. K. 2013. High thermal sensitivity of blood enhances oxygen delivery in the high-flying bar-headed goose. J Exp Biol 216: 2172–2175. Meir, J. et al. 2019. Reduced metabolism supports hypoxic flight in the high-flying bar-headed goose (Anser indicus). eLife in press. Milsom, W. K. 2011. Cardiorespiratory support of avian flight. J Exp Biol 214: 4071–4072. Milsom, W. K. 2017. Different solutions to restoring oxygen delivery at altitude. Acta Physiol 222: e12926. Mu, C.-Y. et al. 2016. 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https://onlinelibrary.wiley.com/doi/pdf/10.1111/ecog.05170

The challenge of novel abiotic conditions for species undergoing climate‐induced range shifts

Insights into the causal mechanisms that limit species distributions are likely to improve our ability to anticipate species range shifts in response to climate change. For species with complex life histories, a mechanistic understanding of how climate affects different lifecycle stages may be crucial for making accurate forecasts. Here, we use mechanistic niche modeling (NicheMapR) to derive "proximate" (mechanistic) variables for tadpole, juvenile, and adult Rana temporaria. We modeled the hydroperiod, and maximum and minimum temperatures of shallow (30 cm) ponds, as well as activity windows for juveniles and adults. We then used those ("proximate") variables in correlative ecological niche models (Maxent) to assess their role in limiting the species' current distribution, and to investigate the potential effects of climate change on R. temporaria across Europe. We further compared the results with a model based on commonly used macroclimatic ("distal") layers (i.e., bioclimatic layers from WorldClim). The maximum temperature of the warmest month (a macroclimatic variable) and maximum pond temperatures (a mechanistic variable) were the most important range-limiting factors, and maximum temperature thresholds were consistent with the observed upper thermal limit of R. temporaria tadpoles. We found that range shift forecasts in central Europe are far more pessimistic when using distal macroclimatic variables, compared to projections based on proximate mechanistic variables. However, both approaches predicted extensive decreases in climatic suitability in southern Europe, which harbors a significant fraction of the species' genetic diversity. We show how mechanistic modeling provides ways to depict gridded layers that directly reflect the microenvironments experienced by organisms at continental scales, and to reconstruct those predictors without extrapolation under novel future conditions. Furthermore, incorporating those predictors in correlative ecological niche models can help shed light on range-limiting processes, and can have substantial impacts on predictions of climate-induced range shifts.

Integrating mechanistic and correlative niche models to unravel range-limiting processes in a temperate amphibian.

Species ranges are constrained by the physiological tolerances of organisms to climatic conditions. By incorporating physiological constraints, species distribution models can identify how biotic and abiotic factors constrain a species' geographic range. Rates of water loss influence species distributions, but characterizing water loss for an individual requires complex calculations. Skin resistance to water loss (ri) is considered to be the most informative metric of water loss rates because it controls for experimental biases. However, calculating ri requires biophysical equations to solve for the resistance of the air that surrounds an organism, termed the boundary layer resistance (rb). Here, we compared theoretical and empirical methods for measuring skin resistance to water loss of a Plethodon salamander collected from nature. For the empirical methods, we measured rb of agar replicas at five body sizes, two temperatures, three vapor pressure deficits, and six flow rates using a flow-through system. We also calculated rb using biophysical equations under the same experimental conditions. We then determined the ecological implications of incorporating skin and boundary layer resistance into a species range model that estimated potential activity time and energy balance throughout the geographic range of the study species. We found that empirical methods for calculating rb resulted in negative values of ri, whereas biophysical calculations produced meaningful values of ri. The species range model determined that ignoring realistic boundary layer and skin resistances reduced average estimates of energy balance by as much as 64% and potential activity time by 88% throughout the spatial extent of the model. We conclude that the use of agar replicas is an inadequate technique to characterize skin resistance to water loss, and incorporating boundary layer and skin resistances to water loss improves estimates of activity and energetics for mechanistic species distribution models. More importantly, our study suggests that incorporating the physical processes underlying rates of water loss could improve estimates of habitat suitability for many animals.

https://esajournals.onlinelibrary.wiley.com/doi/pdf/10.1002/ecm.1240

Jonathan P. Odom

Papers

Plasticity reveals hidden resistance to extinction under climate change in the global hotspot of salamander diversity

Physical calculations of resistance to water loss improve predictions of species range models