Significance Climate change—especially accelerated warming and drying—threatens to increase extinction risk, yet there is little evidence that physiological limitations have contributed to species declines. This study links species-specific water requirements for cooling body temperature to the collapse of a Mojave Desert bird community over the past century from climate change. Species occupying the hottest, driest sites were less likely to persist. Birds with the greatest water requirements for cooling their body temperature experienced the largest declines. Large-bodied carnivores and insectivores were especially vulnerable to cooling costs because they obtain water primarily from their food. Climate warming increases the evaporative cooling demand for birds, which will affect geographic patterns in body size and future extinction risk.

Abstract Climate change threatens global biodiversity by increasing extinction risk, yet few studies have uncovered a physiological basis of climate-driven species declines. Maintaining a stable body temperature is a fundamental requirement for homeothermic animals, and water is a vital resource that facilitates thermoregulation through evaporative cooling, especially in hot environments. Here, we explore the potential for thermoregulatory costs to underlie the community collapse of birds in the Mojave Desert over the past century in response to climate change. The probability of persistence was lowest for species occupying the warmest and driest sites, which imposed the greatest cooling costs. We developed a general model of heat flux to evaluate whether water requirements for evaporative cooling contributed to species’ declines by simulating thermoregulatory costs in the Mojave Desert for 50 bird species representing the range of observed declines. Bird species’ declines were positively associated with climate-driven increases in water requirements for evaporative cooling and exacerbated by large body size, especially for species with animal-based diets. Species exhibiting reductions in body size across their range saved up to 14% in cooling costs and experienced less decline than species without size reductions, suggesting total cooling costs as a mechanism underlying Bergmann’s rule. Reductions in body size, however, are unlikely to offset the 50 to 78% increase in cooling costs threatening desert birds from future climate change. As climate change spreads warm, dry conditions across the planet, water requirements are increasingly likely to drive population declines, providing a physiological basis for climate-driven extinctions.

Climate change threatens to accelerate the ongoing, rapid loss of biodiversity (1, 2), prompting an urgent need to identify the mechanisms that make species vulnerable (3). Vulnerability to climate change increases when environmental conditions challenge an organism’s capacity to balance heat and water budgets (4), suggesting physiological mechanisms will underlie some population declines (5). However, the physiological bases of climate vulnerability are often inferred indirectly from population declines (6), and empirical evidence supports the uncoupling of species interactions as the most common cause of climate-driven extinctions (7). A major impediment to detecting the physiological bases of climate vulnerability is the complex nature of the organism–climate interaction, especially for endotherms. Heat transfer through avian plumage and mammal pelage complicates our understanding of the homeothermic requirements of endotherms (8, 9). Establishing meaningful links between physiology and long-term population responses to climate change would represent a major advance for predicting endotherm climate vulnerability.

At a fundamental level, energy imbalance between an organism and its environment—manifested as changes in mass, water, and heat—drives climate vulnerability (4). The primary determinants of energy exchange are environmental temperature and body size (10). Body size determines an organism’s total energetic requirements, whereas temperature modulates this relationship (11). Warming temperatures can influence the spatial and temporal patterns in body size by causing local energetic imbalances (12). Large-bodied endotherms, for instance, simultaneously experienced rapid extinction (13) and reductions in body size during Pleistocene warming (14), with analogous patterns occurring in response to human-caused climate change (15). Similar negative associations between body size and average annual temperature have also been reported across species’ geographic ranges in a pattern generally referred to as Bergmann’s rule (16). However, models of heat flux have not supported a mechanistic explanation of Bergmann’s rule (17), possibly due to their focus on the benefits of greater heat retention in large-bodied endotherms inhabiting cool climates. Given that geographic variation in body mass is more strongly associated with maximum than minimum temperatures (18), shifting perspectives to evaluate size-dependent cooling costs in hot environments might produce different insights.

We developed simulation models of heat flux to evaluate whether water requirements for evaporative cooling contributed to the collapse of the Mojave Desert bird community over the last century that has been explicitly linked to climate change (19). Since the original surveys by Joseph Grinnell and others in the early 20th century, Mojave sites, situated mostly within national parks and reserves with minimal land use change, have lost on average 43% of their bird species. Occupancy probability significantly declined for 39 of 135 (29%) breeding birds, while only one species significantly increased. Climate change, particularly a long-term decline in precipitation, was the most important driver of site-level persistence of species (19). Drying conditions should impose the greatest pressure on homeothermy in warming environments by increasing water requirements for cooling, while simultaneously limiting the availability of water. Here, we evaluated the prediction that persistence of bird species over the past century should be lowest at hot, dry sites due to greater water requirements for cooling. We then estimated species-specific cooling requirements in 50 species using a simulation-based approach that linked climate warming to biophysical traits, such as body size, shape, and plumage properties. We focused on cooling costs because water requirements for homeothermy in birds increase exponentially under warm conditions, leading to potentially lethal dehydration under climate change (20). We used our simulations to 1) test whether increases in cooling requirements over the past century were associated with occupancy declines species experienced in the Mojave, and 2) explore cooling requirements as a mechanism underlying Bergmann’s rule.

Conclusions Species interactions are thought to cause most climate-driven extinctions to date (7), partly because the physiological bases of climate vulnerability are complicated by thermodynamic relationships with the environment. By directly modeling the water requirements of desert birds, our study illustrates the importance of an intrinsic, physiological basis of avian decline that is associated with climate change (19). We uncovered greater climate vulnerability in larger species from accelerated water requirements, which was especially relevant for birds with animal-based diets and at sites without surface water. Water requirements are increasingly likely to drive population declines as climate change spreads warm and dry conditions across the planet over the next century (50). Thus, species with large body size, with animal-based diets, and that violate Bergmann’s rule may become more vulnerable globally. Although our study focused on a physiologically challenging desert environment, ecologists can leverage climate–organism interactions to identify the relevance of other intrinsic, physiological factors. In tropical environments, for instance, rising temperatures may predispose ectotherms with high thermal sensitivities to greater climate vulnerability (51). Thus, linking physiology to relevant ecological traits may become a powerful approach to identifying biodiversity vulnerable to climate change.

Acknowledgments We thank the University of California, Berkeley, Museum of Vertebrate Zoology for assistance and permission to use specimens; and Andrew McKechnie and Tom Litwin for reviewing the manuscript. The research was funded by the National Science Foundation (Division of Environmental Biology Grants 1457742 and 1457524).

Footnotes Author contributions: E.A.R., K.J.I., B.O.W., B.S., and S.R.B. designed research; E.A.R. and K.J.I. performed research; E.A.R. and K.J.I. analyzed data; E.A.R., B.O.W., and S.R.B. wrote the paper; and K.J.I. provided critical data.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

Data deposition: The Python script for these simulations has been deposited on GitHub (https://github.com/ecophysiology/cooling_costs). Specimen identification numbers have been deposited on the Open Science Framework (https://osf.io/jtpsf/).

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1908791116/-/DCSupplemental.