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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., (© The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Evaporative cooling is a prerequisite for avian occupancy of hot, arid environments, and is the only avenue of heat dissipation when air temperatures ( T a ) exceed body temperature ( T b ). 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 T a We analyzed variation in three response variables: (1) slope of EWL at T a between 40 and 46°C, (2) EWL at T a =46°C and (3) EHL/MHP at T a =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., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2018. Published by The Company of Biologists Ltd.)

Nightjars represent a model taxon for investigating physiological limits of heat tolerance because of their habit of roosting and nesting in sunlit sites during the heat of the day. We investigated the physiological responses of Rufous-cheeked nightjars (Caprimulgus rufigena) and Freckled nightjars (Caprimulgus tristigma) to high air temperatures (T a ) by measuring body temperature (T b ), resting metabolic rate (RMR) and total evaporative water loss (TEWL) at T a ranging from 10 to 56 °C. Both species became hyperthermic at T a  > T b . Lower critical limits of thermoneutrality occurred at T a between 35 and 37 °C, whereas we detected no clear upper critical limits of thermoneutrality. Between T a  ≈ 37.0 and 39.9 °C, rates of TEWL increased rapidly with T a . At T a  ≥ 40 °C, fractional increases in mass-specific TEWL rates were 78-106% of allometric predictions. Increasing evaporative heat dissipation incurred only small metabolic costs, with the RMR of neither species ever increasing by more than 20% above thermoneutral values. Consequently, both species displayed extremely efficient evaporative cooling; maximum evaporative heat dissipation was equivalent to 515% of metabolic heat production (MHP) at T a  ≈ 56 °C in C. rufigena and 452% of MHP at T a  ≈ 52 °C in C. tristigma. Our data reiterate that caprimulgids have evolved an efficient mechanism of evaporative cooling via gular fluttering, which minimizes metabolic heat production at high T a and reduces total heat loads. This likely aids in reducing TEWL rates and helps nightjars cope with some of the most thermally challenging conditions experienced by any bird.

Seasonal changes in weather and food availability differentially impact energy budgets of small mammals such as bats. While most thermal physiological research has focused on species that experience extreme seasonal temperature variations, knowledge is lacking from less variable temperate to subtropical climates. We quantified ambient temperature (T a ) and skin temperature (T sk ) responses by individuals from a population of New Zealand lesser short-tailed bats (Mystacina tuberculata) during summer and winter using temperature telemetry. During summer, communal roosts were more thermally stable than T a . During winter, solitary roosts were warmer than T a indicating significant thermal buffering. Communal roost trees were used on 83 % of observation days during summer, and individuals occupying them rarely entered torpor. Solitary roosts were occupied on 93 % of observation days during winter, and 100 % of individuals occupying them used torpor. During summer and winter, bats employed torpor on 11 and 95 % of observation days, respectively. Maximum torpor bout duration was 120.8 h and winter torpor bout duration correlated negatively with mean T a . Torpor bout duration did not differ between sexes, although female minimum T sk was significantly lower than males. The summer Heterothermy Index varied, and was also significantly affected by T a . Mean arousal time was correlated with sunset time and arousals occurred most frequently on significantly warmer evenings, which are likely associated with an increased probability of foraging success. We provide the first evidence that torpor is used flexibly throughout the year by M. tuberculata, demonstrating that roost choice and season impact torpor patterns. Our results add to the growing knowledge that even small changes in seasonal climate can have large effects on the energy balance of small mammals.

In mammals, reproduction, especially for females is energetically demanding. Therefore, during the reproductive period females could potentially adjust patterns of thermoregulation and foraging in concert to minimise the energetic constraints associated with pregnancy and lactation. We assessed the influence of pregnancy, lactation, and post-lactation on torpor use and foraging behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temperature and foraging by tracking bats which carried temperature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the patterns of torpor use varied significantly between reproductive (pregnant and lactating) females and post-lactating females. As we predicted, reproductive females entered torpor for shorter bouts than post-lactating females. Although all females used torpor frequently, pregnant females spent less time in torpor, and maintained higher skin temperatures than either lactating or post-lactating females. This result suggests that delayed offspring development which has been associated with torpor use during pregnancy, may pose a higher risk to an individual's reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged bats did not vary with reproductive condition, suggesting that even short, shallow bouts of torpor produce substantial energy savings, likely obviating the need to spend more time foraging. Our data clearly show that torpor use and reproduction are not mutually exclusive and that torpor use (no matter how short or shallow) is an important means of balancing the costs of reproduction for M. lucifugus.

Australian owlet-nightjars (Aegotheles cristatus; ∼50 g) are one of only a few avian species that roost in cavities year-round and regularly enter torpor. Cavity roosts act as thermal buffers, and roost type likely affects energy expenditure of small birds. We used radiotelemetry to locate diurnal winter roost sites of owlet-nightjars in central Australia and to measure body (T (b)) and skin (T (skin)) temperature. We also recorded ambient temperature inside (T (IN)) and outside roosts. Individual owlet-nightjars used one to seven different roosts (tracking time 3-10 weeks), selecting either rock crevices (four birds) or tree hollows (four birds), or switching between the two roost types (seven birds). Rock crevices (T (IN) +9°C to +33°C) were warmer and thermally more stable than tree hollows (T (IN) -4.0°C to +37°C). Torpor, often expressed by a reduction of T (skin)/T (b) by >10°C for 3-4 h at dawn, was influenced by roost selection; torpor use in tree hollows was almost twice that in rock crevices. Despite the potential energy savings accrued from roosting in well-insulated cavities, owlet-nightjars roosted in tree hollows more often (65% bird days, n = 398) than in rock crevices (35% bird days, n = 211). Lower costs of arousal from torpor via passive rewarming and basking and decreased risk of predation are two possible explanations for the preference to roost in tree hollows. We provide the first evidence for the influence of cavity roost selection on torpor use in a free-ranging bird and show that roost selection and thermal biology are strongly interrelated in determining energy expenditure.

Many studies have shown that endotherms become more heterothermic when the costs of thermoregulation are high and/or when limited energy availability constrains thermoregulatory capacity. However, the roles of many ecological variables, including constraints on foraging opportunities and/or success, remain largely unknown. To test the prediction that thermoregulatory patterns should be related to foraging opportunities in a heterothermic endotherm, we examined the relationship between the lunar cycle and heterothermy in Freckled Nightjars (Caprimulgus tristigma), which are visually orienting, nocturnal insectivores that are dependent on ambient light to forage. This model system provides an opportunity to assess whether variation in foraging opportunities influences the expression of heterothermy. The nightjars were active and foraged for insects when moonlight was available but became inactive and heterothermic in the absence of moonlight. Lunar illumination was a much stronger predictor of the magnitude of heterothermic responses than was air temperature (T(a)). Our data suggest that heterothermy was strongly related to variation in foraging opportunities associated with the lunar cycle, even though food abundance appeared to remain relatively high throughout the study period. Patterns of thermoregulation in this population of Freckled Nightjars provide novel insights into the environmental and ecological determinants of heterothermy, with the lunar cycle, and not T(a), being the strongest predictor of torpor use.

Most studies of hibernation physiology sample individuals from populations within a single geographic area, yet some species have large ranges meaning populations likely experience area-specific levels of energetic challenges. As well, few studies have assessed within-season variation. Since physiological adjustments often are influenced by environmental factors, and the types of environments vary with geography, we expected variance in hibernation patterns among geographically separated populations. Our specific goal was to measure intraspecific variation in torpid metabolic rate (TMR) and body temperature (T (b)) as a function of ambient temperature (T (a)) for a non-migratory and migratory species to determine whether there is a continuum in physiological responses based on latitude. We chose big brown (Eptesicus fuscus) and eastern red bats (Lasiurus borealis) as model species and sampled individuals from populations throughout each species' winter range. In both species, individuals from southern populations maintained higher TMR at cooler T (a)s and lower TMR at warmer T (a)s than those from northern populations. Big brown bats from southern populations regulated T (b) during torpor at higher levels and there was no significant difference in T (b) between populations of eastern red bats. Although metabolic responses were similar across the gradient between species, the effect was more dramatic in big brown bats. Our data demonstrate a continuum in thermoregulatory response, ranging from classic hibernation in northern populations to a pattern more akin to daily torpor in southern populations. Our research highlights the potential usefulness of bats as model organisms to address questions about within-species physiological variation in wild populations.

Altricial mammals and birds become endothermic at about half the size of adults and presumably would benefit energetically from entering torpor at that time. Because little is known about torpor during development in endotherms, we investigated whether after the establishment of endothermic thermoregulation (i.e. the ability to maintain a high body temperature during cold exposure), Sminthopsis macroura, a small (approximately 25 g) insectivorous marsupial, is capable of entering torpor and whether torpor patterns change with growth. Endothermic thermoregulation was established when the nest young reached a body mass of approximately 10 g, and they were capable of entering torpor early during development at approximately 10-12 g, lending some support to the view that torpor is a phylogenetically old mammalian trait. Torpor bout length shortened significantly and the minimum metabolic rate during torpor increased as juveniles approached adult size, and consequently total daily energy expenditure increased steeply with age. Relationships between total daily energy expenditure and body mass during development of S. macroura (slope approximately 1.3) differed substantially from the relationship between basal metabolism and body mass in adult endotherms (slope approximately 0.75) suggesting that the energy expenditure-size relationship during the development differs substantially from that in adults under thermo-neutral conditions. Our study shows that while torpor can substantially reduce energy expenditure during development of endotherms and hence is likely important for survival during energy bottlenecks, it also may enhance somatic growth when food is limited. We therefore hypothesize that torpor during the development in endotherms is far more widespread than is currently appreciated.

The use of heterothermy is well documented in the order Caprimulgiformes, but there is conflicting information regarding whether whip-poor-wills are heterothermic. Consequently, we sought to rigorously examine the thermoregulatory abilities of this species. Our study was conducted in southeast South Dakota (42 degrees 47'N, 97 degrees 0'W), where 35 individuals were captured and outfitted with external, temperature-sensitive radio transmitters. We found evidence that whip-poor-wills used daily torpor during the autumn of 2000 and the spring of 2001 (n=12 torpor bouts, based on 346 bird-nights of observation). The average minimum skin temperature of two torpid whip-poor-wills (n=5 torpor bouts) in spring 2001 was 20.1 degrees +/-2.6 degrees C, and bouts of reduced skin temperature lasted an average of 360.0+/-93.7 min. The distribution of heterothermy within the Caprimulgiform phylogeny suggests that the trait is ancestral in the order. Specific heterothermic parameters, however, differ among the different species. In particular, the frequency of torpor use in whip-poor-wills is lower than for other species. These data suggest that several factors, including weather conditions and gender-specific reproductive ecology, influence the propensity of whip-poor-wills and other Caprimulgiformes to enter torpor.