Figures
Abstract
The proportion of organisms exposed to warm conditions is predicted to increase during global warming. To better understand how bats might respond to climate change, we aimed to obtain the first data on how use of torpor, a crucial survival strategy of small bats, is affected by temperature in the tropics. Over two mild winters, tropical free-ranging bats (Nyctophilus bifax, 10 g, n = 13) used torpor on 95% of study days and were torpid for 33.5±18.8% of 113 days measured. Torpor duration was temperature-dependent and an increase in ambient temperature by the predicted 2°C for the 21st century would decrease the time in torpor to 21.8%. However, comparisons among Nyctophilus populations show that regional phenotypic plasticity attenuates temperature effects on torpor patterns. Our data suggest that heterothermy is important for energy budgeting of bats even under warm conditions and that flexible torpor use will enhance bats’ chance of survival during climate change.
Citation: Stawski C, Geiser F (2012) Will Temperature Effects or Phenotypic Plasticity Determine the Thermal Response of a Heterothermic Tropical Bat to Climate Change? PLoS ONE 7(7): e40278. https://doi.org/10.1371/journal.pone.0040278
Editor: Frank Seebacher, University of Sydney, Australia
Received: May 2, 2012; Accepted: June 4, 2012; Published: July 3, 2012
Copyright: © 2012 Stawski, Geiser. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: Financial support was provided by an Australian Postgraduate Award, Bat Conservation International, Jagiellonian University and the University of New England to Clare Stawski and the Australian Research Council to Fritz Geiser. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
It is predicted that global warming will expose organisms to new thermal challenges and will result in poleward or altitudinal shifts of animals [1]. While a change in distribution to deal with climate change may be an option for some species, the response of animals is often too slow and not all can move, resulting in mismatching phenologies with potentially detrimental effects [2]–[3]. However, predictions on how animals might respond to climate change often rely on geographic ranges of species and the climate within these [4] and generally assume that species are static and have limited functional flexibility. Contrary to this, endothermic mammals, which have received little attention with regard to climate change [5], may adjust form and function to better suit the thermal conditions they were exposed to during their development [6]–[7]. This is especially true for heterothermic mammals capable of expressing torpor, which are known to be highly flexible in adjusting their energy requirements seasonally and regionally [8]–[13]. Importantly, the phenotypic plasticity of energy expenditure afforded by the opportunistic use of torpor appears to be a key factor in reducing the risk of extinction in mammals [14]–[15] and may be crucial in dealing with climate change and other anthropogenic disturbances.
Heterothermic endotherms use reductions in metabolic rate (MR) and body temperature (Tb) during periods of torpor for energy conservation [16]. Torpor is used by diverse birds and mammals, often when food is limited, but also without apparent energetic stress to enhance fat stores for future energy demanding events, or to avoid predators [17]–[20]. Heterothermy is used by members of more than half of all mammalian orders [14] and is expressed especially in small species because their thermoregulatory energy expenditure can become costly during exposure to low ambient temperatures (Ta).
Torpor use appears paramount in small temperate bats and it is well established that they often express a sequence of multiday torpor bouts (i.e. hibernation) during winter and short bouts of torpor lasting for part of the day in summer [21]–[23]. In contrast, it was believed in the past that bats inhabiting tropical regions do not use torpor at all because of mild environmental conditions [24]. This view is no longer supported because short bouts of torpor have been observed in captive tropical bats [25]–[27], and because subtropical bats express multiday torpor in the wild [28]–[30]. However, in the tropics essentially all information on the use of mammalian torpor in nature is currently limited to dwarf lemurs and tenrecs [31]–[34], despite the enormous diversity of tropical bats. Although bats comprise >20% of all mammals and the vast majority of these live in the tropics [27], only two individuals of a single species have been examined with regard to torpor in the wild [11].
Global warming is predicted to increase the numbers of bats exposed to tropical or at least warm conditions. Because this will affect energy use and foraging requirements, understanding the thermal biology of tropical bats in the wild will provide potential insights into how bats from other climates might respond to climate change. Although an increased Ta will reduce energy expenditure for normothermic thermoregulation at high Tb, if bats do not use torpor at all their energy requirements will be substantially increased even under warm conditions [35]. The purpose of our study was twofold. We (i) aimed to provide the first long-term quantitative data on torpor use and activity patterns in relation to ambient conditions by tropical free-ranging northern long-eared bats, Nyctophilus bifax, that are entirely restricted to subtropical/tropical regions. We (ii) used these data and data from the literature to make predictions about how thermal energetics and torpor patterns of bats from tropical and other climate zones may be affected by climate change.
Materials and Methods
Permits to undertake the research were provided by the UNE Animal Ethics Committee (AEC08/046, AEC09/058) and Queensland Parks and Wildlife Service (WITK04955708). A small subset of the data were published previously [36], however, a substantial amount of new data were added and all were re-analysed.
The field study was undertaken over two consecutive austral winters in June 2008 and July/August 2009 at Djiru National Park (17°50′S, 146°03′E), located in the tropical north of the Australian east coast and within the northern parts of the distribution range of N. bifax [37]. During both years, Ta was measured with temperature data loggers (±0.5°C, iButton thermochron DS1921G, Maxim Integrated Products, Inc., USA) in the shade 2 m above the ground. Thermal conditions during the two winters were similar: the overall mean Ta was 18.8±1.6°C and the mean Ta minima and maxima were 16.4±2.4°C and 21.9±1.7°C, respectively. The lowest and highest Ta recorded was 10.6 and 25.3°C, respectively.
Bats were netted for several hours after sunset. Captured bats were weighed to the nearest 0.1 g using an electronic scale and kept overnight. Captive bats were hand fed with mealworms and given water. On the following afternoon a small patch of fur from between the shoulder blades was removed and a temperature-sensitive radio-transmitter (∼0.5 g, LB-2NT, Holohil Systems Inc., Canada) was glued to the exposed skin using a latex adhesive (SkinBond, Smith and Nephew United, Australia). The pulse rate of these transmitters is temperature-dependent and all transmitters were calibrated to the nearest 0.1°C in a water bath between 5 and 40°C against a precision thermometer before attachment. External transmitters provide a reasonable measure of core Tb as Tskin of resting or torpid small mammals differs by <2°C from core Tb [38]. Transmitters worn and shed by bats (3 in 2008; 1 in 2009) were retrieved and re-calibrated 21 to 26 days after the initial calibration and were within 0.5°C of the initial calibration over the entire temperature range.
Bats were released at their capture site and on the following morning and on every day bats retained the transmitter each individual, identified by the frequency of its transmitter, was radio-tracked to its roost location. To automatically record Tskin every 10 min, remote receiver/loggers with antennae [39] were placed within range of the bats’ transmitter signal. Receiver/loggers were checked every morning when bats were located to ensure transmitter reception. Manual readings of the transmitter signals were taken daily to certify the accuracy of receiver/logger readings. Data from receiver/loggers were downloaded and batteries replaced every three days.
Data were obtained for a total of 35 bat days (n = 7 individuals, 4 females, 3 males; body mass: 10.4±0.7 g) in June 2008. During July/August 2009 data were obtained for a total of 78 bat days (n = 6 individuals, 4 females, 2 males; body mass: 9.9±0.7 g,). Mean body mass did not differ between years (P = 0.3, T = 1.1).
Torpor bouts are often defined as periods with Tb <30°C [40]. As the Tb-Tskin differential during torpor is generally <2°C, we defined torpor bouts as the time when Tskin was <28°C. Data analyses were performed using StatistiXL (V 1.8, 2007); data are reported as means ± SD (n = number of individuals, N = number of observations). Means of each individual were used to calculate means for repeated measures. Results were considered significant when alpha was <0.05. To determine whether timing of arousals and torpor entries differed significantly from random, a Rayleigh test was used. T-tests were used to compare independent means; data of the sexes were pooled because they were statistically indistinguishable. Linear regressions were fitted by the least squares method and ANCOVAs were used to compare linear regressions. If no difference in slope between individuals or study periods was observed, data were pooled and regressed together.
Results
Torpor Patterns
A total of 210 torpor bouts were recorded over both winters. Torpor was used on 83% (June 2008) and 100% (July/August 2009; both years combined 95%) of days on which data were collected. In both years, bats expressed different patterns of thermoregulation, entering 0 to 4 torpor bouts/day; some bats remained torpid for an entire day (5.7% of torpor days; Fig. 1). The two most common temporal patterns were one torpor bout/day (31.1%) and two torpor bouts/day (33.0%), typically with one bout in the morning and the other in the afternoon. Four bouts/day were rare (6.6%), but three bouts/day were relatively common (23.6%; Fig. 1), with the third bout occurring during the night before a possible early morning foraging period.
The patterns shown are (i, Tskin: open circles, Ta: dotted line) an individual that remained torpid during the whole day and aroused only in the evening to possibly forage, and the second pattern shows (ii, Tskin: closed circles, Ta: smooth line) an individual displaying the typical morning and afternoon bouts of torpor along with an additional torpor bout during the night. The horizontal black and white bars at the bottom of the graphs represent night and day, respectively.
Mean torpor bout duration for both winters was 4.5±3.1 h (n = 13, N = 210; years did not differ: P = 0.7, T11 = 0.4). The longest torpor bout recorded was 33.3 h and a total of 31 torpor bouts (out of 210) were >10 h. Torpor bouts were negatively correlated with minimum Ta (R2 = 0.2, P<0.001; Fig. 2). The two longest torpor bouts recorded for each individual were strongly affected by minimum Ta (R2 = 0.8, P<0.001; Fig. 2) and the thermal response for this relationship was pronounced (Q10 = 10).
All torpor bouts recorded are represented by the open circles and dashed line (log10 TBD = 2.1–0.09[Ta °C]; R2 = 0.2, P<0.001, F1,209 = 55.0). The two longest bouts recorded for each individual are represented by the closed circles and solid line (log10 TBD = 2.7 - 0.1[Ta °C]; R2 = 0.8, P<0.001, F1,25 = 73.3).
Skin Temperature
Mean daily minimum Tskin in torpid N. bifax during both winters was 20.1±3.1°C (n = 13, N = 102; years did not differ: P = 0.1, T11 = 1.8). The lowest individual Tskin value recorded was 11.3°C (Ta = 10.6°C). The daily minimum torpid Tskin was correlated with Ta (R2 = 0.5, P<0.001; Fig. 3). The mean differential between daily minimum Tskin during torpor and the corresponding Ta was 2.1±1.7°C (n = 13, N = 101; years did not differ: P = 0.7, T6 = 0.4).
This relationship is represented by the following equation: minimum Tskin(°C) = 2.4+1.0[Ta°C]; R2 = 0.5, P<0.001, F1,100 = 101.2.
Timing of Torpor and Activity
Entries into torpor in 2008 (Fig. 4) displayed a peak at a mean time (angle) of 8∶14±5∶10 h (n = 7, N = 43); in 2009 the mean time was 2∶50±5∶15 h (n = 6, N = 167; 2009), but timing of torpor entries did not differ significantly from random (2008: Rayleigh Z = 0.3, P = 0.2; 2009: Z = 0.5, P = 0.2). Arousals were non-randomly distributed in 2008 (Z = 6.0, P = 0.002) with a mean time of 16∶20±4∶17 h (n = 7, N = 43), but not in 2009 (mean: 15∶02±5∶04 h, n = 6, N = 167, Z = 2.5, P = 0.1). Evening arousals likely for foraging occurred at sunset ±00∶06 h (n = 7, N = 22; 2008) and slightly before sunset 00∶06±00∶04 h (n = 6, N = 60; 2009). The proportion of a night N. bifax remained normothermic during both winters was positively correlated with mean nightly Ta (R2 = 0.4, P<0.001; Fig. 5).
Distribution of times of arousals from torpor (top half of graphs) and entries into torpor (bottom half of graphs) of N. bifax during (A) June 2008 and (B) July/August 2009 relative to the time of sunset (0 hours). Each individual contributed several points to these graphs, ranging from 2 to 41 data points. Each bar represents a 30 minute period. The horizontal black and white bars at the top and bottom of the graphs represent night and day, respectively.
This relationship is represented by the following equation: proportion night normothermic = −0.9+0.09[Ta °C]; R2 = 0.4, P<0.001, F1,95 = 51.1.
Discussion
Our study provides the first long-term quantitative data of torpor use and patterns in a tropical bat in its natural environment. It also is the first to show that tropical bats can remain torpid for >1 day. While this was a rare occurrence, torpor was frequently used (95% of all study days) even though weather conditions were mild. Our extensive field study of N. bifax and a recent brief field study on two individual N. geoffroyi during winter in a tropical habitat [11] confirm earlier findings from laboratory work [25]–[26] that torpor is indeed widely used by tropical bats for energy conservation in the wild. Further, data on tropical bats and on other mammals such as lemurs and tenrecs from Madagascar [31]–[33] show that, contrary to the widely held view, torpor use is prevalent in tropical regions. Frequent use of torpor by bats during winter in tropical regions, as reported here for N. bifax, highlights the importance of energy conservation for small microbats even under relatively mild conditions.
Several different patterns of torpor were expressed by N. bifax during both winters, with a peak in arousals from torpor bouts just before sunset. The variation in use of torpor by N. bifax is likely in response to variations in weather conditions and food abundance and N. bifax were normothermic/active longer on warmer nights like other bat species [23], [30]. For insectivorous bats specifically it makes sense to use more torpor at low Ta to save energy when feeding is difficult. In the current study torpor bout duration at minimum Tas >14°C varied widely above and below the regression line, whereas at minimum Tas <14°C all torpor bouts fell above the regression line (Fig. 2). This effect of Ta may reflect insect availability, which decreased significantly at Tas <16°C in the study region [41]. It is also important to note in this context that the thermal response of torpor bout duration of N. bifax was pronounced (Q10 = 10), which is about 3-fold of that usually observed in temperate bats (Q10 = 2.6 to 3.9, [42]). This high thermal sensitivity will permit tropical N. bifax to use relatively long torpor bouts in response to a small reduction of Ta and, on the other hand, be active for much of the night when Ta increases.
The Tskin of torpid N. bifax approached Ta, with a minimum Ta-Tskin differential of ∼2°C. Even on particularly cold days when Tskin was very low, bats apparently continued to thermo-conform because the Ta-Tskin differential remained constant suggesting that torpid bats did not thermoregulate. The lowest Tskin recorded was 11.3°C, which is rather low for a tropical mammal and suggests that individuals of this population of N. bifax can approximate the low Tbs that are characteristic of hibernation in cold climates [16], [35]. This is supported by laboratory data showing that tropical N. bifax commenced to thermoregulate during torpor only at Ta 6.7°C and the minimum Tb was 7.3°C [43]. Therefore, the generally high Tskin in the current study compared to cold-climate hibernators appears to be mainly a reflection of the high Tas bats experienced. However, the minimum Tb measured in the laboratory was also somewhat higher than in temperate hibernators and this trait appears to be selected by the Ta animals are exposed to in the wild [8], [36].
What are the implications of our data for the effect of climate change on bats? We used two approaches to assess this: (i) We assumed that the thermal physiology of bats is constant and estimated using data from the present study and published data [43] how a predicted Ta increase by 2°C will affect torpor patterns and consequently energy use, and (ii) used data on thermal biology from free-ranging subtropical and temperate Nyctophilus populations to test these predictions.
If we (i) use data presented here and those on thermal energetics of tropical N. bifax [43], we can estimate energy expenditure during torpor from mean Tskin and MR regressions because the animals were thermo-conforming and rewarmed largely passively, in comparison to normothermic thermoregulation over the same time period. At a mean Ta of 18.8°C, N. bifax remained torpid for 33.5% of the time, or 8.02 h/day, with a mean Tskin of 24.3°C during torpor using 525 J (assuming 19.7 kJ/lO2 for metabolised fat, [44]). Resting normothermic bats at Ta 18.8°C would have used 7,710 J, and the energy saved by using torpor would be 7,185 J (895.8 J/h) or 28% of the daily energy expenditure of a 10-g temperate bat (25.88 kJ/d, [45]). The thermal response of torpor bout duration (Fig. 2) predicts that a 2°C increase in Ta will shorten the duration of torpor to 21.8% of the time (5.23 h/day), and energy expenditure during torpor will be 467 J. Resting normothermic bats at Ta 20.8°C would need less energy for thermoregulation (4,131 J) and energy savings due to torpor would decrease to 3,664 J (700 J/h) or 14% of the predicted daily energy expenditure [45]. Thus, even at the higher Ta, energy savings by using torpor are substantial and biologically meaningful.
Pronounced discrepancies were observed when we (ii) examined whether and how the thermal biology of populations of bat species in the wild differs from that predicted from regressions. In N. bifax mean torpor bout duration of a subtropical population [36] is predicted to decrease from 3.0 to 1.8 h if Ta increases by 2°C from the tropical mean minimum Ta of 16.4°C to 18.4°C (Fig. 2, 6). However, measured torpor bout duration at the tropical site at Ta 16.4°C is in fact 3.8 h (127% of predicted) and 2.4 h at Ta 18.4°C (136% of predicted). This shows that temperature effects on torpor bout duration vary among populations and suggests that either the tropical bats have acclimated or have been selected to maintain relatively long torpor bouts at warm Ta. Measured and predicted values differ even more in the congener N. geoffroyi (Fig. 6), distributed over almost the entire Australian continent. Data from N. geoffroyi from a temperate region in summer [22] predict that torpor bout duration at the mean minimum Ta of 19.2°C in tropical Northern Territory is only 1.7 h and will decline to 1.2 h with a 2°C rise of Ta. Measured torpor bout duration in tropical N. geoffroyi at a mean minimum Ta of 19.2°C is in fact 4.9 h [11], 2.8-times that predicted from temperate bats. Winter data [23] predict that torpor bout duration of temperate N. geoffroyi at a minimum Ta of 19.2°C and a mean Tskin of 26.2°C is only 1.0 h, only 21% of that measured in the tropics.
Measured (black bars) and predicted (white and grey bars) torpor bout duration in tropical and subtropical N. bifax (A), and in tropical and temperate N. geoffroyi (B). Measured values are those obtained at the tropical sites at the mean minimum Ta (Ta 16.4°C and Ta 16.4+2°C N. bifax, Ta 19.2°C only for N. geoffroyi because no Ta-torpor bout duration regression is available). Predicted torpor bout durations were calculated from regressions in subtropical N. bifax [36] and from temperate N. geoffroyi in summer (white bars, [22]) and winter (grey bar, [23]).
As torpor is usually associated with cold, whereas climate change with global warming, what do our projections actually tell us about bats in a warming climate? During periods of high temperatures, heat waves are known to induce hyperthermia and can kill large pteropodid bats [46]. However, pteropodids comprise only a rather small number (∼20%) of bat species and many large members of this family may roost at exposed sites often directly affected by Ta extremes. In contrast, most ‘microbats’ roost in sheltered areas like caves, mines, houses, under bark or leaves that are buffered from thermal extremes, and, in addition to using torpor, can also be tolerant of extremely high Ta exceeding 50°C [47]. Thus, our and previously available data suggest that by using torpor opportunistically and by being able to tolerate high Ta, small bats may be better equipped to deal with climate change than is predicted from bio-climatic data, especially those species that can shift their distribution to cooler habitats [48].
Obviously, there will be a limit to how far Ta can rise before torpor will become ineffective and a tolerance of high Ta will be exceeded. Moreover, some hibernating mammals are restricted to mountain tops that do not permit further altitudinal adjustments to climate change [2], [49]. Consequently, those heterothermic mammals with a period of winter dormancy that is strongly dependent on historical phenological patterns, which are also often those restricted to limited mountain habitats, are likely to be adversely affected. Recent evidence also shows that hibernating bats are susceptible to new pathogens, such as white-nose syndrome, which kills bats by interfering with their seasonal hibernation [50]. In contrast, opportunistic heterothermic species and those able to use torpor efficiently even under varying thermal conditions, may be able to deal with climate change and other detrimental factors better than predictions from current models might suggest.
Acknowledgments
We thank Alexander Foster, Gerhard Körtner, Alexander Riek and Margaret Stawski for their help with field work.
Author Contributions
Conceived and designed the experiments: CS FG. Performed the experiments: CS FG. Analyzed the data: CS FG. Contributed reagents/materials/analysis tools: CS FG. Wrote the paper: CS FG.
References
- 1. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322: 690–692.
- 2. Inouye DW, Barr B, Armitage KB, Inouye BD (2000) Climate change is affecting altitudinal migrants and hibernating species. P Natl Acad Sci USA 97: 1630–1633.
- 3. Visser ME (2012) Birds and butterflies in climate debt. Nature Clim Change 2: 77–78.
- 4. Kearney M, Porter W (2009) Mechanistic modelling: combining physiological and spatial data to predict species’ range. Ecol Lett 12: 334–350.
- 5. Boyles JG, Seebacher F, Smit B, McKechnie AE (2011) Adaptive thermoregulation in endotherms may alter responses to climate change. Integr Comp Biol 51: 676–690.
- 6. Heath M, Ingram DL (1983) Thermoregulatory heat production in cold-reared and warm-reared pigs. Am J Physiol 244: R273–R278.
- 7. Riek A, Geiser F (2012) Developmental phenotypic plasticity in a marsupial mammal. J Exp Biol 215: 1552–1558.
- 8. Geiser F, Ferguson C (2001) Intraspecific differences in behaviour and physiology: effects of captive breeding on patterns of torpor in feathertail gliders. J Comp Physiol B 171: 569–576.
- 9. Dunbar MB, Brigham RM (2010) Thermoregulatory variation among populations of bats along a latitudinal gradient. J Comp Physiol B 180: 885–893.
- 10. Canale CI, Henry P-Y (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Climate Res 43: 135–147.
- 11. Geiser F, Stawski C, Bondarenco A, Pavey CR (2011) Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals? Naturwissenschaften 98: 447–452.
- 12. Zervanos SM, Maher CR, Waldvogel JA, Florant GL (2010) Latitudinal differences in the hibernation characteristics of woodchucks (Marmota monax). Physiol Biochem Zool 83: 135–141.
- 13. Turbill C, Bieber C, Ruf T (2011) Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc R Soc B 278: 3355–3363.
- 14. Geiser F, Turbill C (2009) Hibernation and daily torpor minimize mammalian extinctions. Naturwissenschaften 96: 1235–1240.
- 15. Liow LH, Fortelius M, Lintulaakso K, Mannila H, Stenseth NC (2009) Lower extinction in sleep-or-hide mammals. Am Nat 173: 264–272.
- 16. Boyer BB, Barnes BM (1999) Molecular and metabolic aspects of mammalian hibernation. Bioscience 49: 713–724.
- 17. Carpenter FL, Hixon MA (1988) A new function for torpor: fat conservation in a wild migrant hummingbird. Condor 90: 373–378.
- 18. Bieber C, Ruf T (2009) Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften 96: 165–17.
- 19. Stawski C, Geiser F (2010) Fat and fed: frequent use of summer torpor in a subtropical bat. Naturwissenschaften 97: 29–35.
- 20.
Geiser F, Brigham RM (2012) The other functions of torpor. In: Ruf T, Bieber C, Arnold W, Millesi E, editors. pp. 109–121. Berlin Heidelberg: Springer-Verlag.
- 21.
Speakman JR, Thomas DW (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton MB, editors. pp. 430–492. Chicago: University of Chicago Press.
- 22. Turbill C, Körtner G, Geiser F (2003) Natural use of torpor by a small, tree-roosting bat during summer. Physiol Biochem Zool 76: 868–876.
- 23. Turbill C, Geiser F (2008) Hibernation by tree-roosting bats. J Comp Physiol B 178: 597–605.
- 24.
Henshaw RE (1970) Thermoregulation in bats. In: Slaughter BH, Walton DW, editors. pp. 188–232. Dallas: Southern Methodist University Press.
- 25. Bartels W, Law BS, Geiser F (1998) Daily torpor and energetics in a tropical mammal, the northern blossom-bat Macroglossus minimus (Megachiroptera). J Comp Physiol B 168: 233–239.
- 26. Kelm DH, von Helversen O (2007) How to budget metabolic energy: torpor in a small Neotropical mammal. J Comp Physiol B 177: 667–677.
- 27. Geiser F, Stawski C (2011) Hibernation and torpor in tropical and subtropical bats in relation to energetics, extinctions, and the evolution of endothermy. Integr Comp Biol 51: 337–348.
- 28. Stawski C, Turbill C, Geiser F (2009) Hibernation by a free-ranging subtropical bat (Nyctophilus bifax). J Comp Physiol B 179: 433–441.
- 29. Cory Toussaint D, McKechnie AE, van der Merwe M (2010) Heterothermy in free-ranging male Egyptian free-tailed bats (Tadarida aegyptiaca) in a subtropical climate. Mammal Biol 75: 466–470.
- 30. Liu J-N, Karasov WH (2011) Hibernation in warm hibernacula by free-ranging Formosan leaf-nosed bats, Hipposideros terasensis, in subtropical Taiwan. J Comp Physiol B 181: 125–135.
- 31. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429: 825–826.
- 32. Lovegrove BG, Génin F (2008) Torpor and hibernation in a basal placental mammal the lesser hedgehog tenrec Echinops telfairi. J Comp Physiol B 178: 691–698.
- 33. Schmid J, Speakman JR (2009) Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests. Naturwissenschaften 96: 609–620.
- 34. McKechnie AE, Mzilikazi N (2011) Heterothermy in Afrotropical mammals and birds: a review. Integr Comp Biol 51: 349–363.
- 35. Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu Rev Physiol 66: 239–274.
- 36.
Stawski C (2012) Comparisons of variables of torpor between populations of a hibernating subtropical/tropical bat from different latitudes. In: Ruf T, Bieber C, Arnold W, Millesi E, editors. pp. 99–108. Berlin Heidelberg: Springer-Verlag.
- 37.
Churchill S (2008) Crows Nest: Allen and Unwin. Australian Bats, 2nd edn.
- 38. Barclay RMR, Kalcounis MC, Crampton LH, Stefan C, Vonhof MJ, et al. (1996) Can external radiotransmitters be used to assess body temperature and torpor in bats? J Mammal 77: 1102–1106.
- 39. Körtner G, Geiser F (2000) Torpor and activity patterns in free-ranging sugar gliders Petaurus breviceps (Marsupialia). Oecologia 123: 350–357.
- 40. Barclay RMR, Lausen CL, Hollis L (2001) What’s hot and what’s not: defining torpor in free-ranging birds and mammals. Can J Zool 79: 1885–1890.
- 41. Richards GC (1989) Nocturnal activity of insectivorous bats relative to temperature and prey availability in tropical Queensland. Aust Wildlife Res 16: 151–158.
- 42. Twente JW, Twente J, Brack V (1985) The duration of the period of hibernation of three species of vespertilionid bats. II Laboratory studies. Can J Zool 63: 2955–2961.
- 43. Stawski C, Geiser F (2011) Do season and distribution affect thermal energetics of a hibernating bat endemic to the tropics and subtropics? Am J Physiol 301: R542–R547.
- 44.
Schmidt-Nielsen K (1997) Animal Physiology. Cambridge: Cambridge University Press.
- 45. Nagy KA, Girard IA, Brown TK (1999) Energetics of free-ranging mammals, reptiles and birds. Annu Rev Nutr 19: 247–277.
- 46. Welbergen JA, Klose SM, Markus N, Eby P (2008) Climate change and the effects of temperature extremes on Australian flying foxes. Proc R Soc B 275: 419–425.
- 47. Maloney SK, Bronner GN, Buffenstein R (1999) Thermoregulation in the Angolan free-tailed bat Mops condylurus: A small mammal that uses hot roosts. Physiol Biochem Zool 72: 385–396.
- 48. Humphries MM, Thomas DW, Speakman JR (2002) Climate-mediated energetic constraints on the distribution of hibernating mammals. Nature 418: 313–316.
- 49. Geiser F, Broome LS (1993) The effect of temperature on the pattern of torpor in a marsupial hibernator. J Comp Physiol B 163: 133–137.
- 50. Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, et al. (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci 109: 6999–7003.