Evolution of avian heat tolerance: The role of atmospheric humidity.

The role of atmospheric humidity in the evolution of endotherms' thermoregulatory performance remains largely unexplored, despite the fact that elevated humidity is known to impede evaporative cooling capacity. Using a phylogenetically informed comparative framework, we tested the hypothesis that pronounced hyperthermia tolerance among birds occupying humid lowlands evolved to reduce the impact of humidity-impeded scope for evaporative heat dissipation by comparing heat tolerance limits (HTLs; maximum tolerable air temperature), maximum body temperatures (Tbmax), and associated thermoregulatory variables in humid (19.2 g H2O m-3) versus dry (1.1 g H2O m-3) air among 30 species from three climatically distinct sites (arid, mesic montane, and humid lowland). Humidity-associated decreases in evaporative water loss and resting metabolic rate were 27%-38% and 21%-27%, respectively, and did not differ significantly between sites. Decreases in HTLs were significantly larger among arid-zone (mean ± SD = 3.13 ± 1.12°C) and montane species (2.44 ± 1.0°C) compared to lowland species (1.23 ± 1.34°C), with more pronounced hyperthermia among lowland (Tbmax = 46.26 ± 0.48°C) and montane birds (Tbmax = 46.19 ± 0.92°C) compared to arid-zone species (45.23 ± 0.24°C). Our findings reveal a functional link between facultative hyperthermia and humidity-related constraints on evaporative cooling, providing novel insights into how hygric and thermal environments interact to constrain avian performance during hot weather. Moreover, the macrophysiological patterns we report provide further support for the concept of a continuum from thermal specialization to thermal generalization among endotherms, with adaptive variation in body temperature correlated with prevailing climatic conditions.

An evaluation of a biophysical model for predicting avian thermoregulation in the heat.

Survival and reproduction of endotherms depend on their ability to balance energy and water exchange with their environment, avoiding lethal deficits and maximising gains for growth and reproduction. At high environmental temperatures, diurnal endotherms maintain body temperature (Tb) below lethal limits via physiological and behavioural adjustments. Accurate models of these processes are crucial for predicting effects of climate variability on avifauna. We evaluated the performance of a biophysical model (NicheMapR) for predicting evaporative water loss (EWL), resting metabolic rate (RMR) and Tb at environmental temperatures approaching or exceeding normothermic Tb for three arid-zone birds: southern yellow-billed hornbill (Tockus leucomelas), southern pied babbler (Turdoides bicolor) and southern fiscal (Lanius collaris). We simulated metabolic chamber conditions and compared model outputs with thermal physiology data collected at air temperatures (Tair) between 10 and 50°C. Additionally, we determined the minimum data needed to accurately model diurnal birds' thermoregulatory responses to Tair using sensitivity analyses. Predicted EWL, metabolic rate and Tb corresponded tightly with observed values across Tair, with only minor discrepancies for EWL in two species at Tair≈35°C. Importantly, the model captured responses at Tair=30-40°C, a range spanning threshold values for sublethal fitness costs associated with sustained hot weather in arid-zone birds. Our findings confirm how taxon-specific parameters together with biologically relevant morphological data can accurately model avian thermoregulatory responses to heat. Biophysical models can be used as a non-invasive way to predict species' sensitivity to climate, accounting for organismal (e.g. physiology) and environmental factors (e.g. microclimates).

Avian Heterothermy: A Review of Patterns and Processes.

Many birds reduce rest-phase energy demands through heterothermy, physiological responses involving facultative, reversible reductions in metabolic rate and body temperature (Tb). Here, we review the phylogenetic distribution and ecological contexts of avian heterothermy. Heterothermy has been reported in 140 species representing 15 orders and 39 families. Recent work supports the view that deep heterothermy is most pronounced in phylogenetically older taxa whereas heterothermy in passerines and other recently diverged taxa is shallower and confined to minimum Tb > 20°C. The reasons why deep heterothermy is absent in passerines remain unclear; we speculate an evolutionary trade-off may exist between the capacity to achieve low heterothermic Tb and the tolerance of hyperthermic Tb. Inter- and intraspecific variation in heterothermy is correlated with factors including foraging ecology (e.g., territoriality and defense of food resources among hummingbirds), food availability and foraging opportunities (e.g., lunar phase predicts torpor use in caprimulgids), and predation risk. Heterothermy also plays a major role before and during migration. Emerging questions include the magnitude of energy savings associated with heterothermy among free-ranging birds, the role phylogenetic variation in the capacity for heterothermy has played in evolutionary radiations into extreme habitats, and how the capacity for heterothermy affects avian vulnerability to rapid anthropogenic climate change.

Respirometry protocols for avian thermoregulation at high air temperatures: stepped and steady-state profiles yield similar results.

Relationships between air temperature (Tair) and avian body temperature (Tb), resting metabolic rate (RMR) and evaporative water loss (EWL) during acute heat exposure can be quantified through respirometry using several approaches. One involves birds exposed to a stepped series of progressively increasing Tair setpoints for short periods (<20-30 min), whereas a second seeks to achieve steady-state conditions by exposing birds to a single Tair for longer periods (>1-2 h). To compare these two approaches, we measured Tb, RMR and EWL over Tair=28°C to 44°C in the dark-capped bulbul (Pycnonotus tricolor). The two protocols yielded indistinguishable values of Tb, RMR and EWL and related variables at most Tair values, revealing that both are appropriate for quantifying avian thermal physiology during heat exposure over the range of Tair in the present study. The stepped protocol, however, has several ethical and practical advantages.

Adaptive variation in the upper limits of avian body temperature.

Physiological performance declines precipitously at high body temperature (Tb), but little attention has been paid to adaptive variation in upper Tb limits among endotherms. We hypothesized that avian maximum tolerable Tb (Tbmax) has evolved in response to climate, with higher Tbmax in species exposed to high environmental heat loads or humidity-related constraints on evaporative heat dissipation. To test this hypothesis, we compared Tbmax and related variables among 53 bird species at multiple sites in South Africa with differing maximum air temperature (Tair) and humidity using a phylogenetically informed comparative framework. Birds in humid, lowland habitats had comparatively high Tbmax (mean ± SD = 45.60 ± 0.58 °C) and low normothermic Tb (Tbnorm), with a significantly greater capacity for hyperthermia (Tbmax - Tbnorm gradient = 5.84 ± 0.77 °C) compared with birds occupying cool montane (4.97 ± 0.99 °C) or hot arid (4.11 ± 0.84 °C) climates. Unexpectedly, Tbmax was significantly lower among desert birds (44.65 ± 0.60 °C), a surprising result in light of the functional importance of hyperthermia for water conservation. Our data reveal a macrophysiological pattern and support recent arguments that endotherms have evolved thermal generalization versus specialization analogous to the continuum among ectothermic animals. Specifically, a combination of modest hyperthermia tolerance and efficient evaporative cooling in desert birds is indicative of thermal specialization, whereas greater hyperthermia tolerance and less efficient evaporative cooling among species in humid lowland habitats suggest thermal generalization.