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 (Tb max), and associated thermoregulatory variables in humid (19.2 g H2 O m-3 ) versus dry (1.1 g H2 O 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 (Tb max = 46.26 ± 0.48°C) and montane birds (Tb max = 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.

Sub-lethal impacts of lead poisoning on blood biochemistry, immune function and delta-aminolevulinic acid dehydratase (δ-ALAD) activity in Cape (Gyps coprotheres) and white-backed (G. africanus) Vulture chicks.

Although the prevalence of lead poisoning in southern Africa's Gyps vultures is now well-established, its finer physiological effects on these endangered species remain poorly characterised. We evaluated the sub-lethal impact of acute lead exposure on Cape and White-backed Vulture chicks from two breeding colonies in South Africa, by analysing its possible effects on key blood biochemistry parameters, immune function, packed cell volume and δ-aminolevulinic acid dehydratase (δ-ALAD) activity. All 37 White-backed Vulture nestlings sampled displayed elevated lead levels (>10 µg/dL), and seven had blood [Pb] >100 µg/dL. Eight of 28 Cape Vulture nestlings sampled had blood [Pb] exceeding background exposure, with one showing blood [Pb] >100 µg/dL. Delta-aminolevulinic acid dehydratase (δ-ALAD) activity was significantly and negatively related to blood [Pb] in nestlings from both species, with 50% inhibition of the enzyme predicted to occur at blood [Pb] = 52.8 µg/dL (White-backed Vulture) and 18.8 µg/dL (Cape Vulture). Although no significant relationship was found between % packed cell volume (PCV) and blood [Pb], the relatively lower mean PCV of 32.9% in White-backed Vulture chicks, combined with normal serum protein values, is likely indicative of depression or haemolytic anaemia. The leukogram was consistent in both species, although the presence of immature heterophils suggested an inflammatory response in White-backed Vulture chicks with blood [Pb] >100 µg/dL. Values for cholesterol, triglycerides, total serum protein, albumin, globulin, albumin/globulin ratio, alanine aminotransferase (ALT) and gamma-glutamyl transferase (GGT) were consistent with values previously reported. Calcium and phosphorus concentrations suggested no adverse effects on bone metabolism. A significant decrease in urea: uric acid (U:UA) ratio at blood [Pb] >100 µg/dL in White-backed Vulture chicks, brought about by a decrease in urea production, raises the possibility of hepatic abnormality. These results suggest that δ-ALAD activity may serve as a sensitive biomarker of lead toxicity in both species, while highlighting the need to better understand the significant variability in sensitivity that is observed, even between closely related members of the same genus.

Thermal acclimatisation to heatwave conditions is rapid but sex-specific in wild zebra finches.

Under climate change, increasing air temperature average and variability pose substantial thermal challenges to animals. While plasticity in thermoregulatory traits could potentially attenuate this impact, whether thermal acclimatisation can occur quickly enough to track weather variability in hot climates is unknown in any endotherm, and sex differences have never been tested. We investigated acclimatisation responsiveness of male and female wild zebra finches to short-term (< 2 weeks) summer temperature fluctuations in the Australian desert. Hotter weather before respirometry trials triggered a typical acclimatisation response (especially at chamber temperature Tchamb ≥ 40). However, acclimatisation occurred remarkably rapidly: metabolic rate responded within just one day, while body temperature (Tb) and evaporative cooling capacity (EHL/MHP) were best predicted by weather on the trial day; whereas evaporative water loss responded more slowly (1 week). Nonetheless, rapid acclimatisation only occurred in males, and females had higher Tb and lower EHL/MHP than males, potentially increasing hyperthermia risk. Furthermore, acclimatisation did not translate into greater acute heat tolerance (i.e. ability to tolerate Tchamb = 46 °C). Our results therefore reveal surprisingly rapid acclimatisation and even anticipatory adjustments to heat. However, with no changes in acute heat tolerance, and in females, phenotypic flexibility may provide only limited buffering against the detrimental impact of heatwaves.

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).

Evidence for a maintenance cost for birds maintaining highly flexible basal, but not summit, metabolic rates.

Reversible phenotypic flexibility allows organisms to better match phenotypes to prevailing environmental conditions and may produce fitness benefits. Costs and constraints of phenotypic flexibility may limit the capacity for flexible responses but are not well understood nor documented. Costs could include expenses associated with maintaining the flexible system or with generating the flexible response. One potential cost of maintaining a flexible system is an energetic cost reflected in the basal metabolic rate (BMR), with elevated BMR in individuals with more flexible metabolic responses. We accessed data from thermal acclimation studies of birds where BMR and/or Msum (maximum cold-induced metabolic rate) were measured before and after acclimation, as a measure of metabolic flexibility, to test the hypothesis that flexibility in BMR (ΔBMR), Msum (ΔMsum), or metabolic scope (Msum - BMR; ΔScope) is positively correlated with BMR. When temperature treatments lasted at least three weeks, three of six species showed significant positive correlations between ΔBMR and BMR, one species showed a significant negative correlation, and two species showed no significant correlation. ΔMsum and BMR were not significantly correlated for any species and ΔScope and BMR were significantly positively correlated for only one species. These data suggest that support costs exist for maintaining high BMR flexibility for some bird species, but high flexibility in Msum or metabolic scope does not generally incur elevated maintenance costs.

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.

Global patterns of climate change impacts on desert bird communities.

The world's warm deserts are predicted to experience disproportionately large temperature increases due to climate change, yet the impacts on global desert biodiversity remain poorly understood. Because species in warm deserts live close to their physiological limits, additional warming may induce local extinctions. Here, we combine climate change projections with biophysical models and species distributions to predict physiological impacts of climate change on desert birds globally. Our results show heterogeneous impacts between and within warm deserts. Moreover, spatial patterns of physiological impacts do not simply mirror air temperature changes. Climate change refugia, defined as warm desert areas with high avian diversity and low predicted physiological impacts, are predicted to persist in varying extents in different desert realms. Only a small proportion (<20%) of refugia fall within existing protected areas. Our analysis highlights the need to increase protection of refugial areas within the world's warm deserts to protect species from climate change.

Identifying the origin of lead poisoning in white-backed vulture (Gyps africanus) chicks at an important South African breeding colony: a stable lead isotope approach.

Elevated lead levels in scavenging raptors can originate from a variety of environmental and anthropogenic sources, including soil, water, mining activities and legacy lead from leaded fuel, but has mostly been attributed to fragments of lead-based ammunition embedded in the tissues of carcasses. To identify the origins of lead in the tissues of white-backed vulture (Gyps africanus) chicks at Dronfield Nature Reserve, South Africa, we used MC-ICP-MS to compare the isotopic composition of lead in blood samples to those of soil in the chicks' immediate environment, different mining activities in South Africa and lead ammunition commonly used in hunting and game management practices. The isotopic ratios in vulture blood samples ranged widely (207Pb/206Pb: 0.827-0.911), but fell within those measured for ammunition (0.761-0.938). Dronfield water can be excluded as a significant source, as the lead concentration for water was below detection limits. Uranium, coal, atmospheric Pb, legacy Pb from fuel and Pb mining can also be excluded as significant sources, based on the limited overlap with Pb isotopic ratios measured in vulture blood. Whereas 55% of chicks we sampled displayed isotopic ratios consistent with Dronfield soil, the low local Pb concentration and the low extractable Pb levels in South African soil in general, imply that soil Pb is unlikely the major source of Pb in WBV chicks, especially in birds with elevated blood Pb levels, i.e. > 20 µg/dL. Our results, when considered in the context of vulture feeding ecology and low Pb levels in non-scavenging birds in South Africa, imply the major source of elevated Pb levels in WBV chicks to be fragments of lead-based ammunition embedded in the carrion fed to them by their parents.

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.

A prenatal acoustic signal of heat affects thermoregulation capacities at adulthood in an arid-adapted bird.

Understanding animal physiological adaptations for tolerating heat, and the causes of inter-individual variation, is key for predicting climate change impacts on biodiversity. Recently, a novel mechanism for transgenerational heat adaptation was identified in a desert-adapted bird, where parents acoustically signal hot conditions to embryos. Prenatal exposure to "heat-calls" adaptively alters zebra finch development and their thermal preferences in adulthood, suggesting a long-term shift towards a heat-adapted phenotype. However, whether such acoustic experience improves long-term thermoregulatory capacities is unknown. We measured metabolic rate (MR), evaporative water loss (EWL) and body temperature in adults exposed to a stepped profile of progressively higher air temperatures (Ta) between 27 and 44 °C. Remarkably, prenatal acoustic experience affected heat tolerance at adulthood, with heat-call exposed individuals more likely to reach the highest Ta in morning trials. This was despite MR and EWL reaching higher levels at the highest Ta in heat-call individuals, partly driven by a stronger metabolic effect of moderate activity. At lower Ta, however, heat-call exposed individuals had greater relative water economy, as expected. They also better recovered mass lost during morning trials. We therefore provide the first evidence that prenatal acoustic signals have long-term consequences for heat tolerance and physiological adaptation to heat.

Phosphorylation status of pyruvate dehydrogenase in the mousebird Colius striatus undergoing torpor.

Torpor is a heterothermic response that occurs in some animals to reduce metabolic expenditure. The speckled mousebird (Colius striatus) belongs to one of the few avian taxa possessing the capacity for pronounced torpor, entering a hypometabolic state with concomitant decreases in body temperature in response to reduced food access or elevated thermoregulatory energy requirements. The pyruvate dehydrogenase complex (PDC) is a crucial site regulating metabolism by bridging glycolysis and the Krebs cycle. Three highly conserved phosphorylation sites are found within the E1 enzyme of the complex that inhibit PDC activity and reduce the flow of carbohydrate substrates into the mitochondria. The current study demonstrates a marked increase in S232 phosphorylation during torpor in liver, heart, and skeletal muscle of C. striatus. The increase in S232 phosphorylation during torpor was particularly notable in skeletal muscle where levels were ~49-fold higher in torpid birds compared to controls. This was in contrast to the other two phosphorylation sites (S293 and S300) which remained consistently phosphorylated regardless of tissue. The relevant PDH kinase (PDHK1) known to phosphorylate S232 was found to be substantially upregulated (~5-fold change) in the muscle during torpor as well as increasing moderately in the liver (~2.2-fold increase). Additionally, in the heart, a slight (~23%) decrease in total PDH levels was noted. Taken together the phosphorylation changes in PDH suggest that inhibition of the complex is a common feature across several tissues in the mousebird during torpor and that this regulation is mediated at a specific residue.

Experimental Manipulation of Air Temperature in Captivity Appears Unsuitable for Evaluating Fecal Glucocorticoid Metabolite Responses of Wild-Caught Birds to Heat Exposure.

AbstractNoninvasive measurement of stress-related alterations in fecal glucocorticoid metabolite (fGCM) concentrations has considerable potential for quantifying physiological responses to very hot weather in free-ranging birds, but practical considerations related to sampling will often make this method feasible only for habituated study populations. Here we evaluate an alternate approach, the use of experimentally manipulated thermal environments for evaluating stress responses to high environmental temperatures in wild-caught birds housed in captivity. Using an enzyme immunoassay utilizing antibodies against 5ß-pregnane-3α,11ß,21-triol-20-one-CMO∶BSA (tetrahydrocorticosterone), we quantified fGCMs in captive individuals of three southern African arid-zone species (southern pied babblers [Turdoides bicolor], white-browed sparrow-weavers [Plocepasser mahali], and southern yellow-billed hornbills [Tockus leucomelas]) experiencing daily air temperature maxima (Tmax) ranging from 30°-32°C to 42°-44°C. For none of the three species did Tmax emerge as a significant predictor of elevated fGCM concentrations, and no stress response to simulated hot weather was evident. The apparent lack of a stress response to Tmax = 42°C in captive southern pied babblers contrasts with linear increases in fGCMs at Tmax > 38°C in free-ranging conspecifics. The lack of an effect of Tmax on fGCM levels may potentially be explained by several factors, including differences in operative temperatures and the availability of water and food between free-ranging and captive settings or the stress effect of captivity itself. Our results suggest that experimental manipulations of thermal environments experienced by wild-caught captive birds have limited usefulness for testing hypotheses concerning the effects of hot weather events on fGCM (and, by extension, glucocorticoid) concentrations.

Dehydration risk is associated with reduced nest attendance and hatching success in a cooperatively breeding bird, the southern pied babbler Turdoides bicolor.

High air temperatures have measurable negative impacts on reproduction in wild animal populations, including during incubation in birds. Understanding the mechanisms driving these impacts requires comprehensive knowledge of animal physiology and behaviour under natural conditions. We used a novel combination of a non-invasive doubly labelled water (DLW) technique, nest temperature data and field-based behaviour observations to test effects of temperature, rainfall and group size on physiology and behaviour during incubation in southern pied babblers Turdoides bicolor, a cooperatively breeding passerine endemic to the arid savanna regions of southern Africa. The proportion of time that clutches were incubated declined as air temperatures increased, a behavioural pattern traditionally interpreted as a benefit of ambient incubation. However, we show that (i) clutches had a <50% chance of hatching when exposed to daily maximum air temperatures of >35.3°C; (ii) pied babbler groups incubated their nests almost constantly (99% of daylight hours) except on hot days; (iii) operative temperatures in unattended nests frequently exceeded 40.5°C, above which bird embryos are at risk of death; (iv) pied babblers incubating for long periods of time failed to maintain water balance on hot days; and (v) pied babblers from incubating groups lost mass on hot days. These results suggest that pied babblers might leave their nests during hot periods to lower the risk of dehydration associated with prolonged incubation at high operative temperatures. As mean air temperatures increase and extreme heat events become more frequent under climate change, birds will likely incur ever greater thermoregulatory costs of incubation, leading to compromised nest attendance and increased potential for eggs to overheat, with implications for nest success and, ultimately, population persistence.

Hot days are associated with short-term adrenocortical responses in a southern African arid-zone passerine bird.

Relatively little effort has been directed towards elucidating the role of physiological stress pathways in mediating avian responses to global heating. For free-ranging southern pied babblers, Turdoides bicolor, daily maximum air temperatures (Tmax) between ∼35 and ∼40°C result in reduced foraging efficiency, loss of body mass and compromised breeding success. We tested the hypothesis that very hot days are experienced as stressors by quantifying relationships between Tmax and faecal glucocorticoid metabolite (fGCM) levels in naturally excreted droppings. On days when Tmax<38°C, fGCM levels were independent of Tmax (mean±s.d. 140.25±56.92 ng g-1 dry mass). At Tmax>38°C, however, fGCM levels increased linearly with Tmax and averaged 190.79±70.13 ng g-1 dry mass. The effects of Tmax on fGCM levels did not carry over to the following morning, suggesting that very hot days are experienced as acute stressors.

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.

Heat tolerance in desert rodents is correlated with microclimate at inter- and intraspecific levels.

Physiological diversity in thermoregulatory traits has been extensively investigated in both endo- and ectothermic vertebrates, with many studies revealing that thermal physiology has evolved in response to selection arising from climate. The majority of studies have investigated how adaptative variation in thermal physiology is correlated with broad-scale climate, but the role of fine-scale microclimate remains less clear . We hypothesised that the heat tolerance limits and evaporative cooling capacity of desert rodents are correlated with microclimates within species-specific diurnal refugia. We tested predictions arising from this hypothesis by comparing thermoregulation in the heat among arboreal black-tailed tree rats (Thallomys nigricauda), Namaqua rock rats (Micaelamys namaquensis) and hairy-footed gerbils (Gerbillurus paeba). Species and populations that occupy hotter diurnal microsites tolerated air temperatures (Ta) ~ 2-4 ℃ higher compared to those species occupying cooler, more thermally buffered microsites. Inter- and intraspecific variation in heat tolerance was attributable to ~ 30% greater evaporative water loss and ~ 44 % lower resting metabolic rates at high Ta, respectively. Our results suggest that microclimates within rodent diurnal refugia are an important correlate of intra- and interspecific physiological variation and reiterate the need to incorporate fine-scale microclimatic conditions when investigating adaptative variation in thermal physiology.