Trade‐offs between water loss and gas exchange influence habitat suitability of a woodland salamander

Abstract

Abstract Reversible acclimation increases resilience to environmental stress, but acclimation may have hidden costs due to underlying linkages between related physiological traits. These linkages might result in trade‐offs that undermine whole‐organism performance if the change in a related trait reduces the net benefits of acclimation or increases susceptibility to alternative environmental stressors. Metabolic rate and water loss rate are two fundamental physiological traits that could interact due to their dependence on gas exchange across shared physical surfaces. Reductions in water loss rate in response to dehydration stress might reduce metabolic rate by constraining the flux of both water and oxygen. We examined acclimation of metabolic rate and water loss rate using a species of woodland salamander (Plethodon metcalfi) in response to temperature and humidity using a full factorial experimental design. We controlled the evaporative demand of the air across temperatures to assess temperature and humidity as independent cues for acclimation. We predicted that reductions in water loss rate would coincide with reductions in metabolic rate in response to temperature due to shared physical and chemical pathways. We also assessed acclimation of heart rates as a potential compensatory mechanism used to promote oxygen delivery. We integrated these responses into a biophysical model developed from first principles to demonstrate the potential for these interactions to influence habitat suitability. We found that reductions in water loss rates during thermal acclimation were associated with simultaneous reductions in metabolic rates, and we did not find a compensatory response in heart rates. We suggest that these linkages underlie whole‐organism strategies (e.g. physiological dormancy or arousal) for reducing the energetic costs imposed by warm temperatures. The biophysical model suggested that the interaction between these two traits potentially structures phenotypic variation in our population because certain combinations of trait values were incapable of reaching positive energy balance. Trade‐offs between linked physiological traits potentially structure whole‐organism strategies for responding to environmental stressors and constrain phenotypic variation. Therefore, predictions of the benefits of acclimation must be interpreted cautiously without knowledge of the underlying trade‐offs among linked physiological traits. A plain language summary is available for this article.