Mapping evaporative water loss in desert passerines reveals an expanding threat of lethal dehydration.

Extreme high environmental temperatures produce a variety of consequences for wildlife, including mass die-offs. Heat waves are increasing in frequency, intensity, and extent, and are projected to increase further under climate change. However, the spatial and temporal dynamics of die-off risk are poorly understood. Here, we examine the effects of heat waves on evaporative water loss (EWL) and survival in five desert passerine birds across the southwestern United States using a combination of physiological data, mechanistically informed models, and hourly geospatial temperature data. We ask how rates of EWL vary with temperature across species; how frequently, over what areas, and how rapidly lethal dehydration occurs; how EWL and die-off risk vary with body mass; and how die-off risk is affected by climate warming. We find that smaller-bodied passerines are subject to higher rates of mass-specific EWL than larger-bodied counterparts and thus encounter potentially lethal conditions much more frequently, over shorter daily intervals, and over larger geographic areas. Warming by 4 °C greatly expands the extent, frequency, and intensity of dehydration risk, and introduces new threats for larger passerine birds, particularly those with limited geographic ranges. Our models reveal that increasing air temperatures and heat wave occurrence will potentially have important impacts on the water balance, daily activity, and geographic distribution of arid-zone birds. Impacts may be exacerbated by chronic effects and interactions with other environmental changes. This work underscores the importance of acute risks of high temperatures, particularly for small-bodied species, and suggests conservation of thermal refugia and water sources.

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: 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 in five Australian passerines reveals within-order biogeographic variation in heat tolerance.

Evaporative heat loss pathways vary among avian orders, but the extent to which evaporative cooling capacity and heat tolerance vary within orders remains unclear. We quantified the upper limits to thermoregulation under extremely hot conditions in five Australian passerines: yellow-plumed honeyeater (Lichenostomus ornatus; ∼17 g), spiny-cheeked honeyeater (Acanthagenys rufogularis; ∼42 g), chestnut-crowned babbler (Pomatostomus ruficeps; ∼52 g), grey butcherbird (Cracticus torquatus; ∼86 g) and apostlebird (Struthidea cinerea; ∼118 g). At air temperatures (Ta) exceeding body temperature (Tb), all five species showed increases in Tb to maximum values around 44-45°C, accompanied by rapid increases in resting metabolic rate above clearly defined upper critical limits of thermoneutrality and increases in evaporative water loss (EWL) to levels equivalent to 670-860% of baseline rates at thermoneutral Ta Maximum cooling capacity, quantified as the fraction of metabolic heat production dissipated evaporatively, ranged from 1.20 to 2.17, consistent with the known range for passerines, and well below the corresponding ranges for columbids and caprimulgids. Heat tolerance limit (HTL, the maximum Ta tolerated) scaled positively with body mass, varying from 46°C in yellow-plumed honeyeaters to 52°C in a single apostlebird, but was lower than that of three southern African ploceid passerines investigated previously. We argue this difference is functionally linked to a smaller scope for increases in EWL above baseline levels. Our data reiterate the reliance of passerines in general on respiratory evaporative heat loss via panting, but also reveal substantial within-order variation in heat tolerance and evaporative cooling capacity.

Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert songbirds.

We examined thermoregulatory performance in seven Sonoran Desert passerine bird species varying in body mass from 10 to 70 g - lesser goldfinch, house finch, pyrrhuloxia, cactus wren, northern cardinal, Abert's towhee and curve-billed thrasher. Using flow-through respirometry, we measured daytime resting metabolism, evaporative water loss and body temperature at air temperatures (Tair) between 30 and 52°C. We found marked increases in resting metabolism above the upper critical temperature (Tuc), which for six of the seven species fell within a relatively narrow range (36.2-39.7°C), but which was considerably higher in the largest species, the curve-billed thrasher (42.6°C). Resting metabolism and evaporative water loss were minimal below the Tuc and increased with Tair and body mass to maximum values among species of 0.38-1.62 W and 0.87-4.02 g H2O h-1, respectively. Body temperature reached maximum values ranging from 43.5 to 45.3°C. Evaporative cooling capacity, the ratio of evaporative heat loss to metabolic heat production, reached maximum values ranging from 1.39 to 2.06, consistent with known values for passeriforms and much lower than values in taxa such as columbiforms and caprimulgiforms. These maximum values occurred at heat tolerance limits that did not scale with body mass among species, but were ∼50°C for all species except the pyrrhuloxia and Abert's towhee (48°C). High metabolic costs associated with respiratory evaporation appeared to drive the limited heat tolerance in these desert passeriforms, compared with larger desert columbiforms and galliforms that use metabolically more efficient mechanisms of evaporative heat loss.

Avian thermoregulation in the heat: efficient evaporative cooling allows for extreme heat tolerance in four southern hemisphere columbids.

Birds show phylogenetic variation in the relative importance of respiratory versus cutaneous evaporation, but the consequences for heat tolerance and evaporative cooling capacity remain unclear. We measured evaporative water loss (EWL), resting metabolic rate (RMR) and body temperature (Tb) in four arid-zone columbids from southern Africa [Namaqua dove (Oena capensis, ∼37 g), laughing dove (Spilopelia senegalensis, ∼89 g) and Cape turtle dove (Streptopelia capicola, ∼148 g)] and Australia [crested pigeon (Ocyphaps lophotes), ∼186 g] at air temperatures (Ta) of up to 62°C. There was no clear relationship between body mass and maximum Ta tolerated during acute heat exposure. Maximum Tb at very high Ta was 43.1±1.0, 43.7±0.8, 44.7±0.3 and 44.3±0.8°C in Namaqua doves, laughing doves, Cape turtle doves and crested pigeons, respectively. In all four species, RMR increased significantly at Ta above thermoneutrality, but the increases were relatively modest with RMR at Ta=56°C being 32, 60, 99 and 11% higher, respectively, than at Ta=35°C. At the highest Ta values reached, evaporative heat loss was equivalent to 466, 227, 230 and 275% of metabolic heat production. The maximum ratio of evaporative heat loss to metabolic production observed in Namaqua doves, 4.66, exceeds by a substantial margin previous values reported for birds. Our results support the notion that cutaneous evaporation provides a highly efficient mechanism of heat dissipation and an enhanced ability to tolerate extremely high Ta.

Avian thermoregulation in the heat: resting metabolism, evaporative cooling and heat tolerance in Sonoran Desert doves and quail.

Birds in subtropical deserts face significant thermoregulatory challenges because environmental temperatures regularly exceed avian body temperature. To understand the differing susceptibility of desert birds to increasing temperatures, we examined thermoregulatory performance and estimated heat tolerance limits (HTLs) for three Sonoran Desert nesting bird species - Gambel's quail, mourning doves and white-winged doves. Using flow-through respirometry we measured daytime resting metabolism, evaporative water loss and real-time body temperature at air temperatures (T(air)) from 30°C to 66°C. We found marked increases in resting metabolism at the upper critical temperature (T(uc)), which was significantly lower in the quail (T(air)=41.1°C) than in both dove species (T(air)=45.9-46.5°C). Gambel's quail maintained low resting metabolic rates and low rates of evaporative water loss at their T(uc) (0.71 W and 1.20 g H2O h(-1), respectively), but were more sensitive to increasing air temperature, reaching their HTL at T(air) of 52°C. Mourning doves and white-winged doves maintained low resting metabolic rates (0.66 and 0.94 W), but higher rates of evaporative water loss (1.91 and 2.99 g H2O h(-1)) at their T(uc) and reached their HTL at T(air) of 58-60°C. Mass-specific evaporative water loss in white-winged doves (147 g) and mourning doves (104 g) was 45% and 30% greater, respectively, than the rate observed in Gambel's quail (161 g) at Tair of 48°C. Higher rates of evaporation and higher T(uc) made the doves exceptionally heat tolerant, allowing them to maintain body temperatures at least 14°C below air temperatures as high as 60°C (140°F).

The impact of humidity on evaporative cooling in small desert birds exposed to high air temperatures.

Environmental temperatures that exceed body temperature (Tb) force endothermic animals to rely solely on evaporative cooling to dissipate heat. However, evaporative heat dissipation can be drastically reduced by environmental humidity, imposing a thermoregulatory challenge. The goal of this study was to investigate the effects of humidity on the thermoregulation of desert birds and to compare the sensitivity of cutaneous and respiratory evaporation to reduced vapor density gradients. Rates of evaporative water loss, metabolic rate, and Tb were measured in birds exposed to humidities ranging from ∼2 to 30 g H2O m(-3) (0%-100% relative humidity at 30°C) at air temperatures between 44° and 56°C. In sociable weavers, a species that dissipates heat primarily through panting, rates of evaporative water loss were inhibited by as much as 36% by high humidity at 48°C, and these birds showed a high degree of hyperthermia. At lower temperatures (40°-44°C), evaporative water loss was largely unaffected by humidity in this species. In Namaqua doves, which primarily use cutaneous evaporation, increasing humidity reduced rates of evaporative water loss, but overall rates of water loss were lower than those observed in sociable weavers. Our data suggest that cutaneous evaporation is more efficient than panting, requiring less water to maintain Tb at a given temperature, but panting appears less sensitive to humidity over the air temperature range investigated here.