Alexander R. Gerson

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

Significance Using measured rates of evaporative water loss, hourly gridded weather data, a 4 °C warming scenario, and physiological models, we show that songbirds in the deserts of the southwestern United States are increasingly susceptible to death from dehydration on hot days. Smaller birds lose water at a proportionally higher rate, and are hence more vulnerable than larger birds to lethal dehydration arising from greater evaporative cooling demands. Our analysis indicates that, by the end of the present century, exposure to potentially lethal conditions could at least quadruple for smaller species. The increasing extent, frequency, and intensity of dehydrating conditions under a warming climate may alter daily activity patterns, geographic range limits, and the conservation status of affected birds. 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 : efficient evaporative cooling allows for extreme heat tolerance in four southern hemisphere columbids

ABSTRACT 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. Summary: Arid-zone pigeons and doves dissipate heat primarily through cutaneous evaporative pathways, which has minimal metabolic costs, is highly efficient and allows for the defense of a relatively low body temperature under extreme heat conditions.

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

ABSTRACT 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 – Gambels 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 (Tair) from 30°C to 66°C. We found marked increases in resting metabolism at the upper critical temperature (Tuc), which was significantly lower in the quail (Tair=41.1°C) than in both dove species (Tair=45.9–46.5°C). Gambels quail maintained low resting metabolic rates and low rates of evaporative water loss at their Tuc (0.71 W and 1.20 g H2O h−1, respectively), but were more sensitive to increasing air temperature, reaching their HTL at Tair 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 Tuc and reached their HTL at Tair 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 Gambels quail (161 g) at Tair of 48°C. Higher rates of evaporation and higher Tuc 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). Highlighted Article: Species-level differences in heat tolerance may drive changes in desert bird communities as global temperatures continue to rise and heat waves become more frequent.

Avian thermoregulation in the heat : evaporative cooling capacity in an archetypal desert specialist, Burchell's sandgrouse (Pterocles burchelli)

ABSTRACT Sandgrouse (Pterocliformes) are quintessential examples of avian adaptation to desert environments, but relatively little is known about the limits to their heat tolerance and evaporative cooling capacity. We predicted that evaporative cooling in Burchells sandgrouse (Pterocles burchelli) is highly efficient and provides the basis for tolerance of very high air temperature (Ta). We measured body temperature (Tb), resting metabolic rate (RMR) and evaporative water loss (EWL) at Ta between 25°C and ∼58°C in birds exposed to successive increments in Ta. Normothermic Tb averaged 39.0°C, lower than typical avian values. At Ta>34.5°C, Tb increased linearly to a maximum of 43.6°C at Ta=56°C. The upper critical limit of thermoneutrality (Tuc) was Ta=43.8°C, closely coinciding with the onset of panting and gular flutter. Above the Tuc, RMR increased 2.5-fold to 2.89 W at Ta=56°C, a fractional increase far exceeding that of many other species under comparable conditions. Rates of EWL increased rapidly at Ta>42.9°C to 7.84±0.90 g h−1 at Ta=56°C, an 11-fold increase above minimal levels. Maximum evaporative cooling efficiency (ratio of evaporative heat loss to metabolic heat production) was 2.03, but could be as high as 2.70 if our assumption that the birds were metabolising lipids is incorrect. Thermoregulation at very high Ta in P. burchelli was characterised by large increases in RMR and EWL, and is much less efficient than in taxa such as columbids and caprimulgids. Summary: Evaporative cooling in Burchells sandgrouse, an archetypal arid-adapted bird, is surprisingly inefficient, and suggestive of heavy reliance on respiratory rather than cutaneous heat dissipation.

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

ABSTRACT 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, Aberts 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 Aberts 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. Summary: Thermoregulatory performance measurements in seven Sonoran Desert passerine bird species show that heat tolerance limits did not scale with body mass among species, but were ∼50°C for all species.

Avian thermoregulation in the heat: evaporative cooling in five Australian passerines reveals within-order biogeographic variation in heat tolerance

ABSTRACT 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. Summary: Five Australian passerines show evaporative cooling mechanisms qualitatively similar to those of other members of the Passeriformes, but have reduced heat tolerance compared with southern African species.

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

ABSTRACT 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. Summary: Caprimulgiformes demonstrate high heat tolerance that is mediated by low rates of resting metabolism and a very efficient evaporative process that uses a gular flutter mechanism.

Comment on an analysis of endotherm thermal tolerances: systematic errors in data compilation undermine its credibility

Understanding the vulnerability of animal populations and communities to rapid climate warming is a critically important endeavour and has recently been informed by a variety of meta-analyses (e.g. [1]). One current area of interest is the synthesis of thermoregulatory data from mammals and birds to examine geographical variation in thermal limits, by comparing thermoregulatory parameters such as thermoneutral zone (TNZ) breadth and variation in the upper and lower critical temperatures that bound the TNZ [2–5]. Here, we report wide-ranging errors in the dataset that is the foundation of Khaliq et al .s [2] analysis. Khaliq et al . [2] presented a large meta-analysis that extracted data on thermoregulation in birds (161 species) and mammals (297 species) from the physiological literature, with the goal of examining the relationships between physiological capacities and geographical variation in climate. From these individual studies, they compiled data on the lower (LCT) and upper (UCT) critical temperatures, which represent the upper and lower boundaries of the TNZ, the range of environmental temperatures over which resting metabolic rate is constant in endothermic homeotherms. Our discovery that many unsuitable or non-existent data had been included in the dataset compiled by Khaliq et al . [2] was initially triggered by our surprise at the large number of mammal UCT data ( N = 297). At the time, we were conducting a comprehensive review of mammalian thermoregulation in the heat and had found far fewer studies (approx. 100) that contained data permitting the determination of a UCT. We then examined the methods section in the electronic supplementary material, figure S1 and accompanying text, which indicated that Khaliq et al . had indeed used the appropriate definitions of LCT and UCT. Given this disparity, we reviewed the source data from …

Data quality problems undermine analyses of endotherm upper critical temperatures

In an analysis of avian and mammalian thermal tolerances recently published in this journal, Khaliq et al. (2015) reported that endotherm thermal niches are phylogenetically conserved in tropical, but not temperate, regions. However, closer examination of the data upon which this analysis was based reveals that many of the upper critical temperature (UCT) data are not valid. Approximately 55% and 42% of avian and mammalian UCT data, respectively, originated from studies in which animals were not exposed to air temperatures high enough to elicit an increase in metabolic rate above minimum levels; the cited UCT values are merely the highest air temperatures at which measurements took place. An additional 18% and 25% of avian and mammalian UCT data, respectively, represent values based on just one individual per species and/or measurements at too few air temperatures above the thermoneutral zone (TNZ) to reliably estimate the UCT. Several recent studies examining global variation in the thermal tolerances of endotherms have focused on the upper and lower limits of the thermoneutral zone (TNZ), the range of air temperatures over which resting metabolic rate is minimal and increments associated with heat production or active heat dissipation are absent. One such study was recently published in this journal; Khaliq and colleagues partitioned variation in thermal traits of mammals and birds into phylogenetic and environmental (i.e. adaptive) components, and reported phylogenetic niche conservatism in tropical, but not temperate, regions (Khaliq et al., 2015). 2424 | CORRESPONDENCE

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

ABSTRACT 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 Burchells 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. Summary: Avian evaporative cooling efficiency and heat tolerance display substantial taxonomic variation that are, unexpectedly, not systematically related to the use of panting versus gular flutter processes.