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).

Daily Torpor in Birds and Mammals: Past, Present, and Future of the Field.

Torpor is an incredibly efficient energy-saving strategy that many endothermic birds and mammals use to save energy, by lowering their metabolic rates, heart rates, and typically body temperatures. Over the last few decades, the study of daily torpor-in which torpor is used for less than 24 hours per bout-has advanced rapidly. The papers in this issue cover the ecological and evolutionary drivers of torpor, as well as some of the mechanisms governing torpor use. We identified broad focus areas that need special attention: clearly defining the various parameters that indicate torpor use and identifying the genetic and neurological mechanisms regulating torpor. Recent studies on daily torpor and heterothermy, including the ones in this issue, have furthered the field immensely. We look forward to a period of immense growth in this field.

Evaporative cooling via panting and its metabolic and water balance costs for lizards in the American Southwest.

In lizards there is considerable variation in the ability to dissipate environmental/endogenous heat loads through evaporative cooling via panting, which effects how long lizards can spend exposed to high solar heat loads. We recently described the differing capacities of lizards to depress body temperature (Tb) through evaporative cooling via panting. Here, we link panting and Tb depression with rates of evaporative water loss and its metabolic costs under high heat loads. We used flow-through respirometry to measure evaporative water loss rates and metabolism of 17 lizard species from the American Southwest while simultaneously measuring Tb. We exposed lizards to air temperatures (Ta) ranging from 35°C to their critical thermal maximum (CTmax) while marking the onset of panting. We then estimated pre-panting Q10 values for metabolism to partition increases in metabolism associated with the van't Hoff effect from the mechanical cost of panting with increasing heat loads. We found that evaporative cooling costs substantially varied among species, with panting effort significantly affecting lizards' evaporative capacity. Lizard evaporation rates ranged from 0.32 to 1.5 g H2O h-1, with individuals losing as much as 6% h-1 of body mass while panting. Lizards also experienced an increase of up to 7.9-fold in metabolic rate while panting, although the overall energetic costs of panting remained relatively low compared with evaporative water costs. Across species, there was a significant positive relationship between the overall rate of evaporative heat loss and the maximum Ta-Tb gradient a species could maintain. While evaporative cooling may be an effective mechanism for reducing Tb and extending activity in hot environments for many species, it has significant metabolic and water balance costs that should be considered, as habitats with high environmental heat loads can be especially costly to an animal's water budgets.

Keeping your cool: thermoregulatory performance and plasticity in desert cricetid rodents.

Small mammals in hot deserts often avoid heat via nocturnality and fossoriality, and are thought to have a limited capacity to dissipate heat using evaporative cooling. Research to date has focused on thermoregulatory responses to air temperatures (Ta) below body temperature (Tb). Consequently, the thermoregulatory performance of small mammals exposed to high Ta is poorly understood, particularly responses across geographic and seasonal scales. We quantified the seasonal thermoregulatory performance of four cricetid rodents (Neotoma albigula, Neotoma lepida, Peromyscus eremicus, Peromyscus crinitus) exposed to high Ta, at four sites in the Mojave Desert. We measured metabolism, evaporative water loss and Tb using flow-through respirometry. When exposed to Ta≥Tb, rodents showed steep increases in Tb, copious salivation and limited evaporative heat dissipation. Most individuals were only capable of maintaining Ta-Tb gradients of ∼1°, resulting in heat tolerance limits (HTLs) in the range Ta=43-45°C. All species exhibited a thermoneutral Tb of ∼35-36°C, and Tb increased to maximal levels of ∼43°C. Metabolic rates and rates of evaporative water loss increased steeply in all species as Ta approached Tb. We also observed significant increases in resting metabolism and evaporative water loss from summer to winter at Ta within and above the thermoneutral zone. In contrast, we found few differences in the thermoregulatory performance within species across sites. Our results suggest that cricetid rodents have a limited physiological capacity to cope with environmental temperatures that exceed Tb and that a rapidly warming environment may increasingly constrain their nocturnal activity.

Thermoregulation in desert birds: scaling and phylogenetic variation in heat tolerance and evaporative cooling.

Evaporative heat dissipation is a key aspect of avian thermoregulation in hot environments. We quantified variation in avian thermoregulatory performance at high air temperatures (Ta) using published data on body temperature (Tb), evaporative water loss (EWL) and resting metabolic rate (RMR) measured under standardized conditions of very low humidity in 56 arid-zone species. Maximum Tb during acute heat exposure varied from 42.5±1.3°C in caprimulgids to 44.5±0.5°C in passerines. Among passerines, both maximum Tb and the difference between maximum and normothermic Tb decreased significantly with body mass (Mb). Scaling exponents for minimum thermoneutral EWL and maximum EWL were 0.825 and 0.801, respectively, even though evaporative scope (ratio of maximum to minimum EWL) varied widely among species. Upper critical limits of thermoneutrality (Tuc) varied by >20°C and maximum RMR during acute heat exposure scaled to Mb0.75 in both the overall data set and among passerines. The slope of RMR at Ta>Tuc increased significantly with Mb but was substantially higher among passerines, which rely on panting, compared with columbids, in which cutaneous evaporation predominates. Our analysis supports recent arguments that interspecific within-taxon variation in heat tolerance is functionally linked to evaporative scope and maximum ratios of evaporative heat loss (EHL) to metabolic heat production (MHP). We provide predictive equations for most variables related to avian heat tolerance. Metabolic costs of heat dissipation pathways, rather than capacity to increase EWL above baseline levels, appear to represent the major constraint on the upper limits of avian heat tolerance.

Nitrogen stable isotope turnover and discrimination in lizards.

RATIONALE: Nitrogen stable isotope ratio (δ15 N) processes are not well described in reptiles, which limits reliable inference of trophic and nutrient dynamics. In this study we detailed δ15 N turnover and discrimination (Δ15 N) in diverse tissues of two lizard species, and compared these results with previously published carbon data (δ13 C) to inform estimates of reptilian foraging ecology and nutrient physiology. METHODS: We quantified 15 N incorporation and discrimination dynamics over 360 days in blood fractions, skin, muscle, and liver of Sceloporus undulatus and Crotaphytus collaris that differed in body mass. Tissue samples were analyzed on a continuous flow isotope ratio mass spectrometer. RESULTS: Δ15 N for plasma and red blood cells (RBCs) ranged between +2.7 and +3.5‰; however, skin, muscle, and liver did not equilibrate, hindering estimates for these somatic tissues. 15 N turnover in plasma and RBCs ranged from 20.7 ± 4 to 303 ± 166 days among both species. Comparison with previously published δ13 C results for these same samples showed that 15 N and 13 C incorporation patterns were uncoupled, especially during winter when hibernation physiology could have played a role. CONCLUSIONS: Our results provide estimates of 15 N turnover rates and discrimination values that are essential to using and interpreting isotopes in studies of diet reconstruction, nutrient allocation, and trophic characterization in reptiles. These results also suggest that somatic tissues can be unreliable, while life history shifts in nutrient routing and metabolism potentially cause 15 N and 13 C dynamics to be decoupled.

Extreme and variable torpor among high-elevation Andean hummingbird species.

Torpor is thought to be particularly important for small endotherms occupying cold environments and with limited fat reserves to fuel metabolism, yet among birds deep torpor is both rare and variable in extent. We investigated torpor in hummingbirds at approximately 3800 m.a.s.l. in the tropical Andes by monitoring body temperature (Tb) in 26 individuals of six species held captive overnight and experiencing natural air temperature (Ta) patterns. All species used pronounced torpor, with one Metallura phoebe reaching a minimum Tb of 3.26°C, the lowest yet reported for any bird or non-hibernating mammal. The extent and duration of torpor varied among species, with overnight body mass (Mb) loss negatively correlated with both minimum Tb and bout duration. We found a significant phylogenetic signal for minimum Tb and overnight Mb loss, consistent with evolutionarily conserved thermoregulatory traits. Our findings suggest deep torpor is routine for high Andean hummingbirds, but evolved species differences affect its depth.

The functional significance of panting as a mechanism of thermoregulation and its relationship to the critical thermal maxima in lizards.

Because most desert-dwelling lizards rely primarily on behavioral thermoregulation for the maintenance of active body temperature, the effectiveness of panting as a thermoregulatory mechanism for evaporative cooling has not been widely explored. We measured changes in body temperature (Tb) with increasing air temperature (Ta) for 17 species of lizards that range across New Mexico and Arizona and quantified the temperatures associated with the onset of panting, and the capacity of individuals to depress Tb below Ta while panting, and estimated the critical thermal maxima (CTmax) for each individual. We examined these variables as a function of phylogeny, body mass and local acclimatization temperature. We found that many species can depress Tb 2-3°C below Ta while panting, and the capacity to do so appears to be a function of each species' ecology and thermal environment, rather than phylogeny. Panting thresholds and CTmax values are phylogenetically conserved within groups. Understanding the functional significance of panting and its potential importance as a thermoregulatory mechanism will improve our understanding of the potential for species' persistence in an increasingly warmer world.

Avian mortality risk during heat waves will increase greatly in arid Australia during the 21st century.

Intense heat waves are occurring more frequently, with concomitant increases in the risk of catastrophic avian mortality events via lethal dehydration or hyperthermia. We quantified the risks of lethal hyperthermia and dehydration for 10 Australian arid-zone avifauna species during the 21st century, by synthesizing thermal physiology data on evaporative water losses and heat tolerance limits. We evaluated risks of lethal hyperthermia or exceedance of dehydration tolerance limits in the absence of drinking during the hottest part of the day under recent climatic conditions, compared to those predicted for the end of this century across Australia. Increases in mortality risk via lethal dehydration and hyperthermia vary among the species modelled here but will generally increase greatly, particularly in smaller species (~10-42 g) and those inhabiting the far western parts of the continent. By 2100 CE, zebra finches' potential exposure to acute lethal dehydration risk will reach ~ 100 d y-1 in the far northwest of Australia and will exceed 20 d y-1 over > 50% of this species' current range. Risks of dehydration and hyperthermia will remain much lower for large non-passerines such as crested pigeons. Risks of lethal hyperthermia will also increase substantially for smaller species, particularly if they are forced to visit exposed water sources at very high air temperatures to avoid dehydration. An analysis of atlas data for zebra finches suggests that population declines associated with very hot conditions are already occurring in the hottest areas. Our findings suggest that the likelihood of persistence within current species ranges, and the potential for range shifts, will become increasingly constrained by temperature and access to drinking water. Our model adds to an increasing body of literature suggesting that arid environments globally will experience considerable losses of avifauna and biodiversity under unmitigated climate change scenarios.

Metabolic rate is negatively linked to adult survival but does not explain latitudinal differences in songbirds.

Survival rates vary dramatically among species and predictably across latitudes, but causes of this variation are unclear. The rate-of-living hypothesis posits that physiological damage from metabolism causes species with faster metabolic rates to exhibit lower survival rates. However, whether increased survival commonly observed in tropical and south temperate latitudes is associated with slower metabolic rate remains unclear. We compared metabolic rates and annual survival rates that we measured across 46 species, and from literature data across 147 species of birds in northern, southern and tropical latitudes. High metabolic rates were associated with lower survival but survival varied substantially among latitudinal regions independent of metabolism. The inability of metabolic rate to explain latitudinal variation in survival suggests (1) species may evolve physiological mechanisms that mitigate physiological damage from cellular metabolism and (2) extrinsic rather than intrinsic sources of mortality are the primary causes of latitudinal differences in survival.

Cooling requirements fueled the collapse of a desert bird community from climate change.

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.

The Physiology of Heat Tolerance in Small Endotherms.

Understanding the heat tolerances of small mammals and birds has taken on new urgency with the advent of climate change. Here, we review heat tolerance limits, pathways of evaporative heat dissipation that permit the defense of body temperature during heat exposure, and mechanisms operating at tissue, cellular, and molecular levels.

Foraging strategies of individual silky pocket mice over a boom-bust cycle in a stochastic dryland ecosystem.

Small mammals use multiple foraging strategies to compensate for fluctuating resource quality in stochastic environments. These strategies may lead to increased dietary overlap when competition for resources is strong. To quantify temporal contributions of high (C3) versus low quality (C4) resources in diets of silky pocket mice (Perognathus flavus), we used stable carbon isotope (δ13C) analysis of 1391 plasma samples collected over 2 years. Of these, 695 samples were from 170 individuals sampled ≥ 3 times across seasons or years, allowing us to assess changes in dietary breadth at the population and individual levels across a boom-bust population cycle. In 2014, the P. flavus population increased to 412 captures compared to 8 captures in prior and subsequent years, while populations of co-occurring small mammals remained stable. As intraspecific competition increased, the population-wide dietary niche of P. flavus did not change, but individual specialization increased significantly. During this period, ~ 27% (41/151) of individuals sampled specialized on C3 resources, which were abundant during the spring and previous fall seasons. Most of the remaining individuals were C3-C4 generalists (64%) (96/151), and only 9% (14/151) specialized on C4 resources. In 2015, P. flavus population density and resource availability declined, individual dietary breadth expanded (84% generalists), no C3 specialists were found, and specialization on C4 resources increased (16%). Our results demonstrate a high degree of inter-individual plasticity in P. flavus foraging strategies, which has implications for how this species will respond to environmental change that is predicted to decrease C3 resources in the future.

Avian thermoregulation in the heat: is evaporative cooling more economical in nocturnal birds?

Evaporative cooling is a prerequisite for avian occupancy of hot, arid environments, and is the only avenue of heat dissipation when air temperatures (Ta) exceed body temperature (Tb). Whereas diurnal birds can potentially rehydrate throughout the day, nocturnal species typically forgo drinking between sunrise and sunset. We hypothesized that nocturnal birds have evolved reduced rates of evaporative water loss (EWL) and more economical evaporative cooling mechanisms compared with diurnal species, permitting nocturnal species to tolerate extended periods of intense heat without becoming lethally dehydrated. We used phylogenetically informed regressions to compare EWL and evaporative cooling efficiency [ratio of evaporative heat loss (EHL) and metabolic heat production (MHP); EHL/MHP] among nocturnal and diurnal birds at high Ta We analyzed variation in three response variables: (1) slope of EWL at Ta between 40 and 46°C, (2) EWL at Ta=46°C and (3) EHL/MHP at Ta=46°C. Nocturnality emerged as a weak, negative predictor, with nocturnal species having slightly shallower slopes and reduced EWL compared with diurnal species of similar mass. In contrast, nocturnal activity was positively correlated with EHL/MHP, indicating a greater capacity for evaporative cooling in nocturnal birds. However, our analysis also revealed conspicuous differences among nocturnal taxa. Caprimulgids and Australian owlet-nightjars had shallower slopes and reduced EWL compared with similarly sized diurnal species, whereas owls had EWL rates comparable to those of diurnal species. Consequently, our results did not unequivocally demonstrate more economical cooling among nocturnal birds. Owls predominately select refugia with cooler microclimates, but the more frequent and intense heat waves forecast for the 21st century may increase microclimate temperatures and the necessity for active heat dissipation, potentially increasing owls' vulnerability to dehydration and hyperthermia.

Avian thermoregulation in the heat: metabolism, evaporative cooling and gular flutter in two small owls.

The thermoregulatory responses of owls to heat stress have been the subject of few studies. Although nocturnality buffers desert-dwelling owls from significant heat stress during activity, roost sites in tree and cactus cavities or in deep shade provide only limited refuge from high environmental temperatures during the day. We measured thermoregulatory responses to acute heat stress in two species of small owls, the elf owl (Micrathene whitneyi) and the western screech-owl (Megascops kennicottii), which occupy the Sonoran Desert of southwestern North America, an area of extreme heat and aridity. We exposed wild-caught birds to progressively increasing air temperatures (Ta) and measured resting metabolic rate (RMR), evaporative water loss (EWL), body temperature (Tb) and heat tolerance limits (HTL; the maximum Ta reached). Comparatively low RMR values were observed in both species, Tb approximated Ta at 40°C and mild hyperthermia occurred as Ta was increased toward the HTL. Elf owls and screech-owls reached HTLs of 48 and 52°C, respectively, and RMR increased to 1.5 and 1.9 times thermoneutral values. Rates of EWL at the HTL allowed for the dissipation of 167-198% of metabolic heat production (MHP). Gular flutter was used as the primary means of evaporative heat dissipation and produced large increases in evaporative heat loss (44-100%), accompanied by only small increases (<5%) in RMR. These small, cavity-nesting owls have thermoregulatory capacities that are intermediate between those of the open-ground nesting nightjars and the passerines that occupy the same ecosystem.

Avian thermoregulation in the heat: phylogenetic variation among avian orders in evaporative cooling capacity and heat tolerance.

Little is known about the phylogenetic variation of avian evaporative cooling efficiency and heat tolerance in hot environments. We quantified thermoregulatory responses to high air temperature (Ta) in ∼100-g representatives of three orders, namely, the African cuckoo (Cuculus gularis, Cuculiformes), lilac-breasted roller (Coracias caudatus, Coraciiformes) and Burchell's starling (Lamprotornis australis, Passeriformes). All three species initiated respiratory mechanisms to increase evaporative heat dissipation when body temperature (Tb) approached 41.5°C in response to increasing Ta, with gular flutter observed in cuckoos and panting in rollers and starlings. Resting metabolic rate and evaporative water loss increased by quantitatively similar magnitudes in all three species, although maximum rates of evaporative water loss were proportionately lower in starlings. Evaporative cooling efficiency [defined as the ratio of evaporative heat loss (EHL) to metabolic heat production (MHP)] generally remained below 2.0 in cuckoos and starlings, but reached a maximum of ∼3.5 in rollers. The high value for rollers reveals a very efficient evaporative cooling mechanism, and is similar to EHL/MHP maxima for similarly sized columbids which very effectively dissipate heat via cutaneous evaporation. This unexpected phylogenetic variation among the orders tested in the physiological mechanisms of heat dissipation is an important step toward determining the evolution of heat tolerance traits in desert birds.

Avian thermoregulation in the heat: evaporative cooling capacity and thermal tolerance in two Australian parrots.

Avian orders differ in their thermoregulatory capabilities and tolerance of high environmental temperatures. Evaporative heat loss, and the primary avenue whereby it occurs, differs amongst taxa. Although Australian parrots (Psittaciformes) have been impacted by mass mortality events associated with extreme weather events (heat waves), their thermoregulatory physiology has not been well characterized. We quantified the upper limits to thermoregulation under extremely hot conditions in two Australian parrots: the mulga parrot (Psephotellus varius; ∼55 g) and the galah (Eolophus roseicapilla; ∼265 g). At air temperatures (Ta) exceeding body temperature (Tb), both species showed increases in Tb to maximum values around 43-44°C, accompanied by rapid increases in resting metabolic rate above clearly defined upper critical limits of thermoneutrality and increases in evaporative water loss to levels equivalent to 700-1000% of baseline rates at thermoneutral Ta Maximum cooling capacity, quantified as the fraction of metabolic heat production dissipated evaporatively, ranged from 1.71 to 1.79, consistent with the known range for parrots, similar to the corresponding range in passerines, and well below the corresponding ranges for columbids and caprimulgids. Heat tolerance limit (the maximum Ta tolerated) ranged from 44 to 55°C, similar to the range reported for passerines, but lower than that reported for columbids and caprimulgids. Our data suggest that heat tolerance in parrots is similar to that in passerines. We argue that understanding how thermoregulatory capacity and heat tolerance vary across avian orders is vital for predicting how climate change and the associated increase in frequency of extreme weather events may impact avian populations in the future.

Avian thermoregulation in the heat: evaporative cooling capacity of arid-zone Caprimulgiformes from two continents.

Birds in the order Caprimulgiformes (nightjars and allies) have a remarkable capacity for thermoregulation over a wide range of environmental temperatures, exhibiting pronounced heterothermy in cool conditions and extreme heat tolerance at high environmental temperatures. We measured thermoregulatory responses to acute heat stress in three species of Caprimulgiformes that nest in areas of extreme heat and aridity, the common poorwill (Phalaenoptilus nuttallii: Caprimulgidae) and lesser nighthawk (Chordeiles acutipennis: Caprimulgidae) in the Sonoran Desert of Arizona, and the Australian owlet-nightjar (Aegotheles cristatus: Aegothelidae) in the mallee woodlands of South Australia. We exposed wild-caught birds to progressively increasing air temperatures (Ta) and measured resting metabolic rate (RMR), evaporative water loss (EWL), body temperature (Tb) and heat tolerance limit (HTL; the maximum Ta reached). Comparatively low RMR values were observed in all species (0.35, 0.36 and 0.40 W for the poorwill, nighthawk and owlet-nightjar, respectively), with Tb approximating Ta at 40°C and mild hyperthermia occurring as Ta reached the HTL. Nighthawks and poorwills reached HTLs of 60 and 62°C, respectively, whereas the owlet-nightjar had a HTL of 52°C. RMR increased gradually above minima at Ta of 42, 42 and 35°C, and reached 1.7, 1.9 and 2.0 times minimum resting values at HTLs in the poorwill, nighthawk and owlet-nightjar, respectively. EWL increased rapidly and linearly as Ta exceeded Tb and resulted in maximum rates of evaporative heat dissipation equivalent to 237-424% of metabolic heat production. Bouts of gular flutter resulted in large transient increases in evaporative heat loss (50-123%) accompanied by only small increments in RMR (<5%). The cavity-nesting/roosting owlet-nightjar had a lower HTL and less efficient evaporative cooling compared with the species that nest and/or roost on open desert surfaces. The high efficiency of gular flutter for evaporative cooling, combined with mild hyperthermia, provides the physiological basis for defending Tb well below Ta in extreme heat and is comparable to the efficient cooling observed in arid-zone columbids in which cutaneous EWL is the predominant cooling pathway.