• Energy Research

SynopsisIntraspecific variation can be as great as variation across species, but the role of intraspecific variation in driving local and large-scale patterns is often overlooked, particularly in the field of thermal biology. In amphibians, which depend on environmental conditions and behavior to regulate body temperature, recognizing intraspecific thermal trait variation is essential to comprehensively understanding how global change impacts populations. Here, we examine the drivers of micro- and macrogeographical intraspecific thermal trait variation in amphibians. At the local scale, intraspecific variation can arise via changes in ontogeny, body size, and between the sexes, and developmental plasticity, acclimation, and maternal effects may modulate predictions of amphibian performance under future climate scenarios. At the macrogeographic scale, local adaptation in thermal traits may occur along latitudinal and elevational gradients, with seasonality and range-edge dynamics likely playing important roles in patterns that may impact future persistence. We also discuss the importance of considering disease as a factor affecting intraspecific variation in thermal traits and population resilience to climate change, given the impact of pathogens on thermal preferences and critical thermal limits of hosts. Finally, we make recommendations for future work in this area. Ultimately, our goal is to demonstrate why it is important for researchers to consider intraspecific variation to determine the resilience of amphibians to global change.

AbstractClimate change is increasing variability in precipitation patterns in many parts of the globe. Unpredictable changes in water availability can be particularly challenging for organisms that rely on precipitation‐fed water sources for completing their life cycle, such as many amphibian species. Although developmental plasticity can mitigate the impacts of changing environments for some species, this strategy can come at a cost to other fitness‐linked traits, such as immune function. We investigated localized variation in the capacity to respond to pond drying and evaluated whether developmental responses induced carry‐over effects in disease susceptibility in three leopard frog species (Rana [Lithobates] pipiens and Rana sphenocephala; two populations each, and one population of Rana chiricahuensis). Using mesocosms located near the site of collection (<15 km away) in five regions spanning a latitudinal gradient, we raised tadpoles under simulated fast drying, slow drying, or constant water levels. After metamorphosis, we characterized several aspects of the skin microbiome, immune function, and response to exposure to the fungal pathogen Batrachochytrium dendrobatidis (Bd). Note that for R. chiricahuensis, the only carry‐over effect measured was response to Bd exposure, for which we observed no effects of pond drying. We found that developmental plasticity in response to drying was rare, except in the southernmost population of R. sphenocephala. In this location, tadpoles responded by accelerating development, and frogs with shorter larval periods developed more severe infections following Bd exposure post‐metamorphosis, suggesting a trade‐off between surviving pond drying and pathogen defense investment. In the three other locations, a lack of accelerated metamorphosis in drying treatments was accompanied by increased mortality, decreased anti‐Bd function of the microbiome, and/or greater Bd infection after exposure. Overall, results suggest that faster drying conditions will likely have negative impacts on amphibians with long larval periods, both directly and indirectly via carry‐over effects. Because effects of drying exposure were not uniform within a species, our findings suggest that local responses may not be generalizable to other regions of the range. These multifaceted effects of climate change on pathogen defenses are increasingly relevant as emerging infectious diseases threaten global biodiversity.

Environmental challenges early in development can result in complex phenotypic trade-offs and long-term effects on individual physiology, performance, and behavior, with implications for disease and predation risk. We examined the effects of simulated pond-drying and elevated water temperatures on development, growth, thermal physiology, and behavior in a widespread North American amphibian, the Southern leopard frog, Rana sphenocephala. Tadpoles were raised in outdoor mesocosms under warming and drying regimes based on projected climatic conditions in 2070. We predicted that amphibians experiencing the rapid pond drying and elevated pond temperatures associated with climate change would accelerate development, be smaller at metamorphosis and demonstrate long-term differences in physiology and exploratory behavior post-metamorphosis. While both drying and warming accelerated development and reduced survival to metamorphosis, only drying resulted in smaller animals at metamorphosis. At approximately one month post-metamorphosis, animals from the control (ambient no-drying) treatment jumped relatively farther at high temperatures in jumping trials. In addition, across all treatments, frogs with shorter larval periods had lower critical thermal minima and maxima. We also found evidence that developing under warming and drying resulted in a less exploratory behavioral phenotype, and that drying, but not warming, resulted in warmer thermal preferences. Furthermore, behavior predicted thermal preference, with less exploratory animals selecting higher temperatures. Our results underscore the multi-faceted effects of early developmental environments on behavioral and physiological phenotypes later in life. For example, thermal preferences can influence disease risk through behavioral thermoregulation, and exploratory behavior may increase risk of predation or pathogen encounter. By impacting thermal physiology, behavior, and various physiological traits, climatic stressors during development may mediate amphibian exposure and susceptibility to predators and pathogens into adulthood. Please see publication for full details regarding data collection and analysis.