Bat thermoregulation in the heat: seasonal variation in evaporative cooling capacities in four species of European bats.

Phenotypic flexibility is an important source of physiological variation in endotherms and plays an integral role in species' response to rapid environmental changes. Studies of phenotypic flexibility have focused on winter acclimatization and cold endurance, and there are fewer data on summer acclimatization and adjustments in heat dissipation capacity, especially in Temperate-Zone species. We used indirect calorimetry and thermometry to test if thermoregulation at high air temperatures (Ta) varies between spring and summer in four species of European vespertilionid bats: Nyctalus noctula, Pipistrellus nathusii, P. pygmaeus, and P. pipistrellus. We measured subcutaneous body temperature (Tsub), evaporative water loss, and resting metabolic rate while exposing bats to a stepped profile of increasing Ta, from 28 °C-48 °C. We predicted that during summer, bats increase heat tolerance and evaporative cooling capacity, to better tolerate hotter Tas. In contrast, we found lower maximum ratios of evaporative heat loss (EHL) to metabolic heat production (MHP) during summer, but no seasonal differences in maximum Ta tolerated or Tsub. The main cause of this seasonal difference in maximum EHL/MHP seems to be from bats increasing EWL more gradually with increasing Ta in summer than spring, particularly in the smaller Pipistrellus species. Therefore, this seasonal variation in heat-dissipation strategies may reflect enhanced water conservation during summer to avoid dehydration, as bats are confined to roosts for longer and hotter days compared to spring.

The heat is on: Thermoregulatory and evaporative cooling patterns of desert-dwelling bats.

For small endotherms inhabiting desert ecosystems, defending body temperatures (Tb) is challenging as they contend with extremely high ambient temperatures (Ta) and limited standing water. In the arid zone, bats may thermoconform whereby Tb varies with Ta, or may evaporatively cool themselves to maintain Tb < Ta. We used an integrative approach that combined both temperature telemetry and flow through respirometry to investigate the ecological and physiological strategies of lesser long-eared bats (Nyctophilus geoffroyi) in Australia's arid zone. We predicted individuals would exhibit desert-adapted thermoregulatory patterns (i.e., thermoconform to prioritise water conservation), and that females would be more conservative with their water reserves for evaporative cooling compared to males. Temperature telemetry data indicated that free-ranging N. geoffroyi were heterothermic (Tskin = 18.9-44.9 °C) during summer and thermoconformed over a wide range of temperatures, likely to conserve water and energy during the day. Experimentally, at high Tas, females maintained significantly lower Tb and resting metabolic rates, despite lower evaporative water loss (EWL) rates compared to males. Females only increased EWL at experimental Ta = 42.5 °C, significantly higher than males (40.7 °C), and higher than any bat species yet recorded. During the hottest day of this study, our estimates suggest the water required for evaporative cooling ranged from 18.3% (females) and 25.5% (males) of body mass. However, if we extrapolate these results to a recent heatwave these values increase to 36.5% and 47.3%, which are likely beyond lethal limits. It appears this population is under selective pressures to conserve water reserves and that these pressures are more pronounced in females than males. Bats in arid ecosystems are threatened by both current and future heatwaves and we recommend future conservation efforts focus on protecting current roost trees and creating artificial standing water sites near vulnerable populations.

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.

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.

How hornbills handle heat: sex-specific thermoregulation in the southern yellow-billed hornbill.

At a global scale, thermal physiology is correlated with climatic variables such as temperature and aridity. There is also evidence that thermoregulatory traits vary with fine-scale microclimate, but this has received less attention in endotherms. Here, we test the hypothesis that avian thermoregulation varies with microclimate and behavioural constraints in a non-passerine bird. Male and female southern yellow-billed hornbills (Tockus leucomelas) experience markedly different microclimates while breeding, with the female sealing herself into a tree cavity and moulting all her flight feathers during the breeding attempt, becoming entirely reliant on the male for provisioning. We examined interactions between resting metabolic rate (RMR), evaporative water loss (EWL) and core body temperature (Tb) at air temperatures (Ta) between 30°C and 52°C in male and female hornbills, and quantified evaporative cooling efficiencies and heat tolerance limits. At thermoneutral Ta, neither RMR, EWL nor Tb differed between sexes. At Ta >40°C, however, RMR and EWL of females were significantly lower than those of males, by ∼13% and ∼17%, respectively, despite similar relationships between Tb and Ta, maximum ratio of evaporative heat loss to metabolic heat production and heat tolerance limits (∼50°C). These sex-specific differences in hornbill thermoregulation support the hypothesis that avian thermal physiology can vary within species in response to fine-scale microclimatic factors. In addition, Q10 for RMR varied substantially, with Q10 ≤2 in some individuals, supporting recent arguments that active metabolic suppression may be an underappreciated aspect of endotherm thermoregulation in the heat.

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.

Phenotypic Plasticity and Local Adaptation in a Wild Hibernator Evaluated through Reciprocal Translocation.

Phenological shifts are the most commonly reported ecological responses to climate change and can be produced rapidly by phenotypic plasticity. However, both the limits of plasticity and whether it will be sufficient to maintain local adaptation (or even lead to maladaptation) are less clear. Increased winter precipitation has been shown to lead to phenological delays and corresponding annual decreases in fitness in Columbian ground squirrels (Urocitellus columbianus). We took advantage of natural phenological variation (across elevations) in this species to better assess the extent of phenotypic plasticity in emergence dates and the relationships between emergence dates and individual annual fitness. We coupled a reciprocal translocation experiment with natural monitoring across two populations separated by ∼500 m in elevation. Individuals in both populations responded plastically to both spring temperature and winter precipitation. Translocated individuals adjusted their emergence dates to approach those of individuals in their adoptive populations but did differ significantly in their emergence dates from residents. There were no differences in annual fitness among treatment groups nor selection on emergence date within a year. Phenotypic plasticity is thus sufficient to allow individuals to respond to broad environmental gradients, but the influence of variation in emergence dates on annual fitness requires further investigation.

The avian "hibernation" enigma: thermoregulatory patterns and roost choice of the common poorwill.

Compared to mammals, there are relatively few studies examining heterothermy in birds. In 13 bird families known to contain heterothermic species, the common poorwill (Phalaenoptilus nuttallii) is the only species that ostensibly hibernates. We used temperature-sensitive radio-transmitters to collect roost and skin temperature (Tskin) data, and winter roost preferences for free-ranging poorwills in southern Arizona. Further, to determine the effect of passive rewarming on torpor bout duration and active rewarming (i.e., the use of metabolic heat to increase Tskin), we experimentally shaded seven birds during winter to prevent them from passively rewarming via solar radiation. Poorwills selected winter roosts that were open to the south or southwest, facilitating passive solar warming in the late afternoon. Shaded birds actively rewarmed following at least 3 days of continuous torpor. Average torpor bout duration by shaded birds was 122 h and ranged from 91 to 164 h. Active rewarming by shaded birds occurred on significantly warmer days than those when poorwills remained torpid. One shaded bird remained inactive for 45 days, during which it spontaneously rewarmed actively on eight occasions. Our findings show that during winter poorwills exhibit physiological patterns and active rewarming similar to hibernating mammals.

Spatiotemporal and demographic variation in the diet of New Zealand lesser short-tailed bats (Mystacina tuberculata).

Variation in the diet of generalist insectivores can be affected by site-specific traits including weather, habitat, and season, as well as demographic traits such as reproductive status and age. We used molecular methods to compare diets of three distinct New Zealand populations of lesser short-tailed bats, Mystacina tuberculata. Summer diets were compared between a southern cold-temperate (Eglinton) and a northern population (Puroera). Winter diets were compared between Pureora and a subtropical offshore island population (Hauturu). This also permitted seasonal diet comparisons within the Pureora population. Lepidoptera and Diptera accounted for >80% of MOTUs identified from fecal matter at each site/season. The proportion of orders represented within prey and the Simpson diversity index, differed between sites and seasons within the Pureora population. For the Pureora population, the value of the Simpson diversity index was higher in summer than winter and was higher in Pureora compared to Eglinton. Summer Eglinton samples revealed that juvenile diets appeared to be more diverse than other demographic groups. Lactating females had the lowest dietary diversity during summer in Pureora. In Hauturu, we found a significant negative relationship between mean ambient temperature and prey richness. Our data suggest that M. tuberculata incorporate a narrower diversity of terrestrial insects than previously reported. This provides novel insights into foraging behavior and ecological interactions within different habitats. Our study is the first from the Southern Hemisphere to use molecular techniques to examine spatiotemporal variation in the diet of a generalist insectivore that inhabits a contiguous range with several habitat types and climates.

Thrifty Females, Frisky Males: Winter Energetics of Hibernating Bats from a Cold Climate.

Mammalian hibernation consists of energy-saving torpor bouts (periods of controlled reduction in body temperature [Tb]) interspersed with brief arousals to normothermic Tb. Frequency and duration of torpor bouts and arousals can affect winter survival and are thought to be influenced by an optimization balancing the energetic benefits of prolonged torpor against the physiological and ecological costs (e.g., accumulation of metabolic wastes). Female little brown bats (Myotis lucifugus) spend their fat reserves more slowly than males during winter, presumably so they can emerge from hibernation in good condition to initiate pregnancy. We used temperature telemetry over three winters to test a prediction of the optimization hypothesis that female M. lucifugus would use longer torpor bouts and/or shorter arousals than males. Females did conserve energy relative to males by adjusting the magnitude and duration of arousals but not the duration of torpor bouts. Although torpor bout duration did not vary by sex for adults, it did vary by age. Adults initially used longer torpor bouts than young-of-the-year, but this difference declined as cave temperature warmed in spring. Males and females in better condition spent more energy during hibernation, again via increased arousal duration rather than decreased torpor bout duration. Longer arousals by males could increase reproductive fitness if males mate with torpid females throughout winter. Our results highlight demographic differences in winter behavior for small hibernators facing extreme energy limitation in cold climates and illustrate the influence that reproductive costs have on hibernation energetics.

Cold and alone? Roost choice and season affect torpor patterns in lesser short-tailed bats.

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.

Host demographic predicts ectoparasite dynamics for a colonial host during pre-hibernation mating.

Parasite dynamics can be mediated by host behaviours such as sociality, and seasonal changes in aggregation may influence risk of parasite exposure. We used little brown bats (Myotis lucifugus) captured during the autumn mating/swarming period to test the hypothesis that seasonal and demographic-based variation in sociality affect ectoparasitism. We predicted that ectoparasitism would: (1) be higher for adult females and young of the year (YOY) than adult males because of female coloniality; (2) increase for adult males throughout swarming because of increasing contact with females; (3) decrease for adult females and YOY throughout swarming because of reduced coloniality and transmission of individual ectoparasites to males; (4) be similar for male and female YOY because vertical transmission from adult females should be similar. Ectoparasitism was lowest for adult males and increased for males during swarming, but some effects of demographic were unexpected. Contrary to our prediction, ectoparasitism increased for adult females throughout swarming and YOY males also hosted fewer ectoparasites compared with adult and YOY females. Interestingly, females in the best body condition had the highest parasite loads. Our results suggest that host energetic constraints associated with future reproduction affect pre-hibernation parasite dynamics in bats.

Warming up and shipping out: arousal and emergence timing in hibernating little brown bats (Myotis lucifugus).

Phenology refers to the timing of events in the annual cycle of organisms. For temperate-zone mammals, hibernation is one such event, but little is known about its phenology. Hibernation consists of energy-saving torpor bouts interspersed with energetically expensive arousals to normothermic Tb, and hibernators should benefit from mechanisms which reduce arousal costs and help them time arousals to coincide with foraging opportunities. In a previous study, we showed that, in contrast to hibernating bats from warmer climates, little brown bats (Myotis lucifugus) from central Canada abandon a circadian pattern to arousal in the middle of winter when there is no chance of feeding. Here, we used temperature telemetry to test whether they would re-synchronize arousals with normal foraging time (i.e. sunset) during late winter as the chance of foraging or emergence opportunities improves, and whether they would synchronize arousals with conspecifics, possibly to exploit social thermoregulation. We also used passive transponders to test whether energy reserves and/or sex differences in reproductive timing influence phenology and the sensitivity of emergence timing to environmental cues. In contrast to patterns in mid-winter, after 7 April 2013, bats synchronized arousals with sunset and with conspecifics. Females emerged earlier than males, and females in the best condition emerged first while body condition had no influence on male emergence timing. Both male and female bats appeared to time emergence with falling barometric pressure, a cue that predicts favourable foraging conditions for bats but which, unlike outside temperature, would have been readily detectable by bats inside the hibernaculum. Our results highlight hibernation traits associated with extreme winter energy limitation for insect-eating bats in cold climates and illustrate the influence of reproductive timing and environmental conditions on hibernation energetics and phenology.

Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation.

For temperate endotherms (i.e., mammals and birds) energy costs are highest during winter but food availability is lowest and many mammals depend on hibernation as a result. Hibernation is made up of energy-saving torpor bouts [periods of controlled reduction in body temperature (T b)], which are interrupted by brief periodic arousals to normothermic T b. What triggers these arousals in free-ranging hibernators is not well understood. Some temperate bats with intermittent access to flying insects during winter synchronize arousals with sunset, which suggests that, in some species, feeding opportunities influence arousal timing. We tested whether hibernating bats from a cold climate without access to food during winter also maintain a circadian rhythm for arousals or whether cues from conspecifics in the same cluster are more important. We used temperature telemetry to monitor skin temperature (T sk) of free-ranging little brown bats (Myotis lucifugus) hibernating in central Manitoba, Canada, where temperatures from 22 October to 22 March were too cold for flying insects. We found no evidence bats synchronized arousals with photoperiod but they did arouse synchronously with other bats in the same cluster. Thus, in the northern part of their range where flying insects are almost never available during winter, little brown bats exhibit no circadian pattern to arousals. Warming synchronously with others could reduce the energetic costs of arousal for individuals or could reflect disturbance of torpid bats by cluster-mates.

Ectoparasite Community Structure of Two Bats (Myotis lucifugus and M. septentrionalis) from the Maritimes of Canada.

Prevalence of bat ectoparasites on sympatric Myotis lucifugus and M. septentrionalis was quantitatively characterized in Nova Scotia and New Brunswick by making systematic collections at swarming sites. Six species of ectoparasite were recorded, including Myodopsylla insignis, Spinturnix americanus, Cimex adjunctus, Macronyssu scrosbyi, Androlaelap scasalis, and an unknown species of the genus Acanthophthirius. Male M. lucifugus and M. septentrionalis had similar prevalence of any ectoparasite (22% and 23%, resp.). Female M. lucifugus and M. septentrionalis had 2-3 times higher prevalence than did conspecific males (68% and 44%, resp.). Prevalence of infection of both genders of young of the year was not different from one another and the highest prevalence of any ectoparasite (M. lucifugus 64%, M. septentrionalis 72%) among all bat groups. Ectoparasite prevalence and intensity varied positively with roost group size and negatively with grooming efficacy and energy budgets, suggesting that these variables may be important in ectoparasite community structure.