J Comp Physiol B (2006) 176: 165–172 DOI 10.1007/s00360-005-0038-7

ORIGINAL PAPER

Christopher Turbill Æ Fritz Geiser Thermal physiology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi

Received: 24 June 2005 / Revised: 13 September 2005 / Accepted: 27 September 2005 / Published online: 6 December 2005 Springer-Verlag 2005

Abstract During roosting in summer, reproductive fe- fact that females roost gregariously whereas male bats male bats appear to use torpor less frequently and at typically roost solitarily. higher body temperatures (Tb) than male bats, ostensi- bly to maximise offspring growth. To test whether field Keywords Bats Æ Energy use Æ Reproduction Æ observations result from differences in thermal physiol- Thermoregulation Æ Torpor ogy or behavioural thermoregulation during roosting, we measured the thermoregulatory response and ener- Abbreviations MR: Metabolic rate Æ RMR: Resting getics of captive pregnant and lactating female and male metabolic rate Æ Ta: Ambient temperature Æ Tb: Body long-eared bats (Nyctophilus geoffroyi 8.9 g and N. temperature Æ TMR: Torpid metabolic rate Æ TNZ: gouldi 11.5 g) during overnight exposure to a constant Thermoneutral zone ambient temperature (Ta)of15C. Bats were captured 1–1.5 h after sunset and measurements began at 21:22±0:36 h. All N. geoffroyi entered torpor com- Introduction mencing at 23:47±01:01 h. For N. gouldi, 10/10 males, 9/10 pregnant females and 7/8 lactating females entered Owing to their small size, insectivorous bats require high torpor commencing at 01:10±01:40 h. The minimum Tb metabolic rates (MR) for thermoregulation at ambient of torpid bats was 15.6±1.1C and torpid metabolic rate temperatures (Ta) below their thermoneutral zone À1 À1 (TMR) was reduced to 0.05±0.02 ml O2 g h .Sexor (TNZ) (Bradley and Deavers 1980). Thermoregulatory reproductive condition of either species did not affect the energy expenditure can therefore be costly over their timing of entry into torpor (F=1.5, df=2, 19, P=0.24), diurnal rest phase (Kurta et al. 1987). This energetic cost minimum TMR (F=0.21, df=4, 40, P=0.93) or mini- is reduced in many bats, however, by entering torpor for mum Tb (F=0.76, df=5, 41, P=0.58). Moreover, sex or part of the roost day during summer and for prolonged reproductive condition did not affect the allometric periods during winter hibernation (e.g. Park et al. 2000; relationship between minimum resting metabolic rate Turbill et al. 2003a). Torpor results in a reduction in and body mass (F=1.1, df=4, 37, P=0.37). Our study body temperature (Tb) to within 1–2CofTa over a wide shows that under identical thermal conditions, thermal range of Ta above the Tb set-point (2C in many physiology of pregnant and lactating female and male temperate bats) and is accompanied by a substantial bats are indistinguishable. This suggests that the ob- depression in MR (Geiser 2004). However, while torpor served reluctance by reproductive females to enter tor- results in large energy savings, the associated low Tb and por in the field is predominantly because of ecological depressed MR impede the normal function of some rather than physiological differences, which reflect the physiological processes. Torpor may be particularly detrimental during reproduction, which usually requires high MR and energy expenditure (Kurta et al. 1987; Kurta et al. 1990; Thompson 1992). Nevertheless, torpor Communicated by I. D. Hume has been observed in a variety of pregnant and lactating C. Turbill (&) Æ F. Geiser mammals (Geiser 1996). In bats, torpor at low Tb slows Centre for Behavioural and Physiological Ecology, Zoology, or interrupts foetal growth during pregnancy (Racey University of New England, Armidale, 1973; Hoying and Kunz 1998) and retards milk pro- NSW 2351, Australia E-mail: [email protected] duction during lactation (Wilde et al. 1999), which can Tel.: +61-2-67732885 lead to reduced postnatal growth rates (Hoying and Fax: +61-2-77733814 Kunz 1998). Torpor may be especially costly for 166 reproductive bats inhabiting the temperate zone where enter torpor during the early morning (Turbill et al. juvenile bats must develop quickly and acquire enough 2003a). During summer torpor, minimum Tskin are often body fat over the short warm season to survive winter around 15C and close to the daily minimum of external hibernation (Racey and Swift 1981; Thomas et al. 1990; Ta. Pregnant and lactating female N. geoffroyi and N. Kunz et al. 1998). gouldi roost in small maternity colonies of 10–20 bats Field studies have found differences in thermoregu- within cavities typically in the trunk of trees (Lumsden latory behaviour among pregnant and lactating female et al. 2002). Preliminary data suggest that in the wild, and male Eptesicus fuscus (Audet and Fenton 1988; females use torpor less frequently than males and have a Hamilton and Barclay 1994; Grinevitch et al. 1995; higher minimum Tb during torpor (Turbill 1999). Lausen and Barclay 2003) and, to a lesser extent, Myotis lucifugus (Chruszcz and Barclay 2002). While repro- ductive female bats regularly enter torpor in summer, Materials and methods they use torpor less frequently and maintain a higher minimum Tb during torpor than male bats at the same Experimental procedures time of the year. In particular, lactating females avoid using deep torpor (a reduction in Tb by >10C) in We used open-flow respirometry to measure the oxygen comparison to pregnant or male bats. The apparent consumption of pregnant and lactating female and male difference in torpor use suggests that pregnant and/or long-eared bats, N. geoffroyi (n=23) and N. gouldi lactating bats differ physiologically from males in their (n=28) during exposure to Ta of 15.0±1.1C overnight thermoregulatory response to low Ta. Alternatively, in captivity. This Ta reflected the minimum Ta experi- thermoregulatory behaviours in the field may reflect enced by males at the field site in summer and allowed a differences in roosting ecology and the use of behavio- decrease of Tb by 20C during torpor. The study was ural thermoregulation by females. In summer, male bats conducted during the Austral spring/summer from 27 typically roost solitarily in poorly insulated roost October to 12 December 2003. Bats were captured using structures (Kunz and Lumsden 2003; Turbill et al. mist nets from Imbota Nature Reserve (3035¢S, 2003a), whereas reproductive female bats congregate in 15141¢E, 1,000 m elevation), located near Armidale on maternity colonies and select warm, insulated roost sites the Northern Tablelands of New South Wales, Austra- (Kerth et al. 2001; Sedgeley 2001; Lourenco and Pal- lia, and immediately transported (10 km) to the labo- meirim 2004). Maternity roosts can also be heated by up ratory at the University of New England. The climate of to 10C above external Ta caused by the release of body the Northern Tablelands is cool-temperate, with an heat by the colony (Dwyer and Harris 1972; Kunz 1974; average daily minimum Ta of 9.8C and a maximum of Hall 1982). Furthermore, females and their young in 24.3C at Armidale during November. Pregnant bats maternity colonies are able to reduce their thermal were identified by gentle palpation of their abdomen for conductance by huddling in a cluster, which can provide the presence of the skull of a foetus and lactating females a 50% reduction in the energetic cost of thermoregu- by the presence of exposed skin surrounding the nipples lation at Ta below the TNZ (Kurta 1985; Kurta et al. and swollen mammary glands visible beneath the skin. 1987; Hayes et al. 1992). Hence, reproductive females Pregnant bats were captured between 27 October and 18 are likely to experience considerably different Ta and November and lactating bats between 13 November and heat loss during roosting than males, which may also 18 December. Measurements of adult male bats were explain apparent differences in their use of torpor. distributed evenly throughout the study period. While it is difficult to accurately measure the Ta Most bats were captured within 1.5 h of sunset (time within occupied roosts and thermal conductance of wild of sunset: 18:12–18:49 h) and measurements of bats in bats (e.g. see Kunz 1974), the thermal physiology of respirometry chambers commenced at 21:22±0:36 h male and reproductive female bats can be compared and not later than 22:48 h. Measurements continued under identical conditions in the laboratory (Studier and overnight and bats were removed from respirometry O’Farrell 1972; Kurta et al. 1987; Cryan and Wolf 2003). chambers the next morning between 08:00 and 09:30 h Assuming that captive bats exhibit natural thermoreg- (average duration of measurements: 11:18±0:41 h). ulatory behaviours (Geiser et al. 2000), the presence or Bats were exposed to the natural photoperiod during lack of physiological differences can be used to predict measurements using a shaded, 15 W incandescent light- the importance of ecological and environmental differ- globe. The Tb of bats was measured (±0.1C) using a ences in roosting conditions to the behaviour of wild digital thermometer (Omega, Stamford, USA) immedi- bats. ately after removing them from the respirometry To assess whether the observed differences are physi- chambers (within 20 s) by inserting a fine calibrated ological or ecological, we tested the thermoregulatory thermocouple 1 cm into the rectum. Bats were weighed response of pregnant and lactating female and male prior to and after the period of measurements, and a Nyctophilus geoffroyi and N. gouldi to cold exposure linear rate of mass loss was assumed for calculation of overnight in captivity. In the field, male N. geoffroyi and mass-specific MR. To identify recaptures, bats were N. gouldi roost solitarily under peeling bark or in other temporarily marked by clipping a small patch of mid- poorly insulated tree structures and in summer frequently dorsal fur. Bats were then placed in cloth bags for the 167 rest of the day and released after dark at their capture for all measurements, which may have resulted in a site. maximum error of ±3%, if the RQ was actually 0.7 or Measurements for several lactating bats that were 1.0 (Withers 1977). Bats were considered to have entered captured early in the lactating period were of a shorter torpor when their oxygen consumption was reduced duration. These bats had given birth recently and their below the published basal MR À1SD for each species young were presumed to have been at risk of dehydra- (Geiser and Brigham 2000). Torpor bouts were clearly tion if left alone in their tree cavity roost over a 24-h demarcated by a distinct and sustained reduction in MR. period. Thus, measurements of females in early lactation Times of arousal were recorded as the first measurement (n=7, N. gouldi; n=1, N. geoffroyi) were completed at of oxygen consumption above basal rates +1SD. Min- 3:30±0:30 h and lasted 6:20±0:27 h. This allowed re- imum resting metabolic rates (RMR) and torpid meta- lease at their capture site prior to dawn (time of sunrise: bolic rates (TMR) were calculated for each individual 4:45–05:03 h). from the average of three relatively stable consecutive measurements (i.e. over 36 min). Minimum RMR values were not obtained from ten bats because they did not Respirometry display stable resting values before entering torpor. Average rate of energy expenditure (kJ hÀ1) of bats was The MR of bats was measured as the rate of oxygen calculated by integrating the whole bat MR over the consumption using open-flow respirometry. Oxygen measurement period. Data from lactating female bats consumption of bats was measured using a single released prior to dawn were excluded from these calcu- channel oxygen analyser (FOX, Sable Systems Interna- lations, as measurements did not occur over the same tional Inc., Las Vegas, USA). The analyser was insulated time period and were not comparable to other bats. within a foam and cardboard box, and located in a Statistical analyses were carried out using Minitab temperature-controlled room (±2C). A sub-sampling Statistical Software V13 to compare variables between design was employed so that the rate of flow of the the species and among sex/reproductive classes within sample air through the analyser remained constant each species. Student’s t test, ANOVA and general linear (125 ml minÀ1) throughout measurements. modelling (GLM) analyses were used to test for signifi- Bats were placed in respirometry chambers (diameter cant differences (P<0.05) among groups. 45 mm, length 100 mm, volume 0.140 l) made from cylindrical, clear Perspex tubes lined internally with plastic mesh and sealed at each end using rubber stop- Results pers containing an inlet and outlet for air. These were hung vertically inside a temperature-controlled cabinet. During exposure to Ta of 15C overnight, all male and A thermocouple was inserted 5 mm into the chamber all pregnant and lactating female N. geoffroyi entered and covered by a plastic lid measured Ta to the nearest torpor (Fig. 1a). In N. gouldi, all males and 9/10 preg- 0.1C. nant and 7/8 lactating females exhibited torpor Outside air was pumped through Silica gel to remove (Fig. 1b). As lactating female N. gouldi were removed moisture and rotameters (Aarlborg 7908, New York, from respirometry chambers early at 3:30 h, it is pos- USA) controlled the rate of airflow to the chambers. sible that the single normothermic lactating bat may After passing through the chambers, excurrent air was have entered torpor had it remained in the respirometer again dried using Silica gel and the rate of airflow was for longer because another lactating N. gouldi entered measured using a mass flow meter (Omega FMA-5606, torpor at 02:36 h, within 30 min of the end of mea- Stamford, USA). A flow rate of 300 ml minÀ1 was used surements. throughout, which was sufficient to maintain the oxygen The time from when bats were placed into chambers content in the excurrent air above 20%. The excurrent until torpor entry did not differ significantly among sex/ air from the three chambers, along with a reference reproductive classes within each species (N. geoffroyi: channel of dried outside air, were sub-sampled in se- F=1.5, df=2, 19, P=0.24; N. gouldi: F=1.1, df=2, 21, quence every 3 min using solenoid values controlled by a P=0.34; Fig. 2). However, relative to the start of mea- computer. Thus, a measurement for each bat was ob- surements, N. geoffroyi entered torpor significantly ear- tained every 12 min. Data from the digital output of the lier (after 2:31±0:55 h) than N. gouldi (03:41±01:42 h) oxygen analyser were used for all measurements and (T=3.0, df=36, P<0.01; Fig. 2). Hence, the average transferred to a computer using a serial connection. The time of torpor entry was 23:47±01:01 h for N. geoffroyi millivolt outputs from the flow meter and the thermo- and 01:10±01:40 h for N. gouldi. After entering torpor, couples and analogue output from the oxygen analyser 11/49 (22%) bats aroused once during the night at were transferred to a computer via a 14 bit A/D con- 03:52±01:20 h and were normothermic for 0:58±0:07 h verter. The analogue data from the analyser were used to before reentering torpor. Arousals occurred in at least calibrate the A/D converter by comparison to the digital one bat from each sex/reproductive class in both species. data before each day of measurements. The proportion of the overall time of measurements Oxygen consumption of bats was calculated using spent in torpor (excluding data for lactating bats that Eq. 3a of Withers (1977). An RQ of 0.85 was assumed were removed early from chambers) was significantly 168

Fig. 1 Metabolic rates of male, pregnant female and lactating female Nyctophilus geoffroyi (a) and N. gouldi (b) during exposure to Ta of 15C overnight in captivity. Dark horizontal bars show time of lights off (natural photoperiod)

greater for N. geoffroyi (78±10%) than for N. gouldi female and lactating female N. geoffroyi (F=1.02, df=2, (67±15%; T=2.5, df=29, P<0.05). The proportion of 19, P=0.38) or between male and pregnant female N. time spent in torpor did not differ among male, pregnant gouldi (T=1.09, df=14, P=0.30). The minimum Tb of all bats that entered torpor was 15.6±1.1C(n=45), which was 0.6±0.6C above Ta. The minimum Tb in torpor did not differ significantly between species (T=0.6, df=44, P=0.6) or among sex/ reproductive classes within each species (F=0.76, df=5, 41, P=0.58). The Tb of the two N. gouldi that remained normothermic were 36.3C (pregnant) and 31.1C (lac- tating). The body mass of bats differed significantly between species (N. geoffroyi: 8.9±1.5 g, N. gouldi: 11.5±2.1 g; T=5.2, df=47, P<0.001) and among sex/reproductive classes within each species (Table 1; N. geoffroyi: F=35.9, df=2, 20, P<0.001; N. gouldi: F=62.9, df=2, 25, P<0.001), with pregnant females having the greatest mass and males the least mass. Owing to the expected allometric relationship be- tween body mass and MR, GLM using log10 body mass as a covariate were fitted to the data to examine differ- ences in log10 RMR and log10 TMR between species and Fig. 2 Time from commencement of measurements until torpor among male, pregnant and lactating female bats within entry by N. geoffroyi and N. gouldi. Two bats, a pregnant and species (Table 1). We found no significant effect of sex/ lactating female N. gouldi, did not enter torpor. Torpor entry reproductive condition on RMR at Ta 15C(F=1.11, occurred significantly earlier in N. geoffroyi than in N. gouldi df=4, 37, P=0.37) and the relationship between RMR (T=3.0, df=36, P<0.01), but did not differ significantly among and body mass (i.e. slope of the line) was the same for males, pregnant females and lactating females within each species (N. geoffroyi: F=1.5, df=2, 19, P=0.24; N. gouldi: F=1.1, df=2, both species (F=0.17, df=1, 35, P=0.68). However, the 21, P=0.34) elevation (y intercept) of this relationship differed sig- 169

Table 1 Body mass, minimum torpid metabolic rate (TMR) and minimum resting metabolic rate (RMR) of male, pregnant female and lactating female Nyctophilus geoffroyi and N. gouldi measured during exposure to Ta of 15C overnight in captivity

Species Sex/condition Mass (g) Minimum TMR Minimum RMR À1 À1 À1 À1 (ml O2 g h ) (ml O2 g h )

N. geoffroyi Lactating 9.0±0.2 (8) 0.05±0.01 (8) 6.74±0.93 (6) Pregnant 10.3±1.2 (8) 0.05±0.02 (8) 5.77±0.76 (4) Male 7.1±0.5 (7) 0.08±0.05 (7) 6.74±0.76 (7) Combined 8.9±1.5 (23) 0.06±0.02 (23) 6.52±0.88 (17) N. gouldi Lactating 11.2±0.7 (8) 0.05±0.02 (5) 5.40±1.01 (6) Pregnant 13.8±1.1 (10) 0.05±0.01 (7) 4.64±0.53 (8) Male 9.3±0.7 (10) 0.05±0.01 (10) 5.51±1.08 (8) Combined 11.5±2.1 (28) 0.05±0.01 (23) 5.15±0.70 (22)

Numbers represent means ± SD for number of individuals in brackets. Bats were exposed to Ta of 15C overnight nificantly between the species (F=6.3, df=1, 36, TMR was not significantly affected by sex/repro- P<0.05), which resulted in parallel fitted lines for each ductive condition (F=0.21, df=4, 40, P=0.93) or spe- species that were significantly related to body mass cies (F=0.08, df=1, 44, P=0.78; Table 1). (F=9.2, df=1, 36, P<0.01; R2=0.55; Fig. 3). Furthermore, TMR was not significantly related to body Notwithstanding the negative relationship observed mass (F=2.85, df=1, 44, P=0.10). The mean minimum À1 À1 between RMR and body mass, the mean RMR of N. TMR at Ta of 15C was 0.059±0.02 ml O2 g h for À1 À1 À1 À1 geoffroyi (6.52±0.9 ml O2 g h ) was significantly N. geoffroyi and 0.050±0.01 ml O2 g h for N. À1 À1 greater than N. gouldi (5.15±1.7 ml O2 g h ; T=4.9, gouldi and means did not differ significantly between the df=24, P<0.001; Table 1). For N. gouldi (but not for N. species (T=1.3, df=27, P=0.20) or among sex/repro- geoffroyi), mean RMR was significantly less for preg- ductive classes within N. geoffroyi (F=1.7, df=2, 20, nant females than other sex/reproductive classes P=0.22) or N. gouldi (F=0.95, df=2, 21, P=0.40; Ta- (F=4.6, df=2, 19, P<0.05). ble 1). As expected, the average rate of energy expenditure (kJ hÀ1) over the measurement period was closely re- lated to the proportion of time spent in torpor (F=124,

Fig. 3 Minimum (log10) resting metabolic rates (RMR) of N. geoffroyi (open symbols) and N. gouldi (filled symbols) exposed to Ta À1 of 15C as a function of (log10) body mass. General linear modeling Fig. 4 Average rate of energy expenditure (kJ h )ofN. geoffroyi (GLM) analyses revealed no significant effect of sex/reproductive (open symbols) and N. gouldi (filled symbols) calculated over the condition on RMR at 15C(F=1.11, df=4, 37, P=0.37) and measurement period (11.3 h). As expected, average energy resulted in parallel fitted lines for each species that were expenditure was closely related to the proportion of time spent in significantly related to body mass (F=9.2, df=1, 36, P<0.01; N. torpor (F=127, df=1, 37, P<0.001; average energy expenditure À1 À1 À1 2 geoffroyi: log10 RMR (ml O2 g h ) = 1.137À0.354·log10 mass (kJ h ) = 1.10À1.04·percentage of time in torpor; R =0.81) and À1 À1 (g), N. gouldi: log10 RMR (ml O2 g h ) = 1.080À0.354·log10 this relationship did not differ significantly between the species mass (g); combined R2=0.55) (F=1.2, df=1, 37, P=0.17) 170 df=1, 37, P<0.001, R2=0.81; Fig. 4). This relationship the sexes in L. cinereus may be required as both male did not differ significantly between the two species and reproductive female bats roost solitarily in open (F=1.2, df=1, 37, P=0.17). Total energy expenditure foliage. Hence, pregnant and lactating female L. cinereus varied from 1.3 kJ for a male N. geoffroyi that spent 87% cannot gain the thermal benefits from roosting in colo- of the measurement time (11.3 h) in torpor to 15.2 kJ nies within insulated structures that are available to for a pregnant N. gouldi that did not enter torpor. most other temperate zone bats. While L. cinereus are selective for roosting sites in foliage that provide a rel- atively warm microclimate (Willis and Brigham 2005), Discussion reproductive females probably experience similar roost Ta to male bats. Consequently, any differences in their Our study shows that sex and reproductive condition natural thermoregulatory behaviours are more likely a have no apparent effect on the thermoregulatory behav- reflection of physiological differences than for other iour, energetics and thermal variables of N. geoffroyi or temperate zone bat species, which have greater scope for N. gouldi during exposure to identical cold conditions selective behavioural means of reducing thermoregula- overnight in captivity. Pregnant and lactating female and tory costs while roosting. male bats within each species responded similarly to cold In addition, the contrasting results may reflect the by entering torpor during the night, as observed in soli- greater thermoregulatory costs of N. geoffroyi and N. tary roosting bats in the wild (Turbill et al. 2003a). gouldi, which are around half to one-third of the body Moreover, because almost all bats entered torpor, mass of L. cinereus. Thermal conductance increases possible nutritional differences at the beginning of logarithmically with decreasing body mass in mammals measurements did not have an apparent effect on the (Bradley and Deavers 1980). In addition, L. cinereus have variables measured. Thus, our results differ from previous a particularly dense pelage that may further reduce their studies and suggest that avoidance of torpor by female thermal conductance (Shump and Shump1980; Cryan reproductive bats in the field is unlikely to be a conse- and Wolf 2003; Willis and Brigham 2005). Hence, mass- quence of difference in thermal physiology, but probably specific RMR of N. geoffroyi and N. gouldi at Ta of 15C results from selection of warm roost microclimates and was approximately 1.4 times greater than in L. cinereus communal roosting during the maternity season. (Cryan and Wolf 2003). For reproductive female N. Our results, showing no difference in thermoregula- geoffroyi and N. gouldi, the energetic cost of defending a tory response between reproductive female and male N. constant, high Tb during exposure to Ta of 15C over- geoffroyi and N. gouldi, are in clear contrast with the night evidently outweighed the benefits to sustaining dichotomous response between pregnant female and foetal growth or milk production. For example, by male captive hoary bats, Lasiurus cinereus, found by employing torpor for an average of 78% of the 11.3 h Cryan and Wolf (2003). These differences may be ex- measurement period, N. geoffroyi reduced their energy plained to some extent by differences in experimental expenditure by approximately 75% from 13.0 to 3.5 kJ. procedures between the studies. In our study, measure- The potential detrimental costs of torpor during ment of captured bats commenced during the night and reproduction are often emphasised, whereas the benefits usually lasted until mid-morning of the next day. Hence, from energy savings to the fitness of mother and young experimental runs lasted >11 h and included the early are possibly underestimated, especially in very small morning when free-ranging bats most often enter torpor endotherms such as bats. Energy expenditure increases naturally (Turbill et al. 2003a). In contrast, measure- during pregnancy to support foetal growth and further ments of L. cinereus took place between 08:00 and increases to reach highest levels during lactation (Racey 16:00 h and experimental runs lasted only 2–4 h (Cryan and Speakman 1987; Kurta et al. 1989, 1990; Thompson and Wolf 2003). As 2–4 h are close to the average time 1992). Thus the use of torpor to reduce thermoregula- prior to torpor entry by Nyctophilus (7–15 g) species in tory energy expenditure may be an important adapta- our study, it seems possible, therefore, that the much tion of small endotherms to maintain a positive energy larger L. cinereus (25–35 g) did not display their natural balance during reproduction. Indeed, McLean and thermal response to low Ta because of the short duration Speakman (1999) found that the daily energy expendi- of measurements. Moreover, measurements of captive L. ture of lactating female bats, Plecotus auritus (8 g) held cinereus were restricted to the daytime, after the time in outdoor aviaries was similar to non-reproductive fe- bats commonly enter their morning torpor bout. The males, indicating that they used energy-saving mecha- possibility that short-term laboratory data were not nisms such as torpor to compensate for the increased representative is further supported by data showing that energy required for lactation. Torpor may be especially pregnant female L. cinereus use torpor frequently while important during sporadic periods of cold or wet roosting under natural conditions in the wild (Hickey weather, when foraging opportunities are reduced and and Fenton 1996; Willis 2005). thermoregulatory costs are high (Hickey and Fenton Nevertheless, the experimental approach by Cryan 1996;Ko¨ rtner and Geiser 2000). Maternity colonies of and Wolf (2003) revealed a marked difference in ther- tree-roosting bats frequently switch between roosts, moregulatory response between male and pregnant during which groups of females may sometimes roost as female bats. A strong physiological difference between individuals or in smaller sub-groups (Kerth and Ko¨ nig 171

1999; Kunz and Lumsden 2003; C. Turbill, unpublished data). Hence, torpor may be used to compensate for References increased thermoregulatory costs at times when repro- ductive females are roosting solitarily or in smaller Audet D, Fenton MB (1988) Heterothermy and the use of torpor by the bat Eptesicus fuscus (Chiroptera: Vespertilionidae): a groups. Using a model of thermoregulatory costs, Cryan field study. Physiol Zool 61:197–204 and Wolf (2003) calculated that the energy expenditure Bradley SR, Deavers DR (1980) A re-examination of the rela- of L. cinereus at Ta of 10C could be reduced by 60% tionship between thermal conductance and body weight in from a torpor bout lasting only 2 h. Most bats are mammals. Comp Biochem Physiol 65A:465–476 Brown CR (1999) Metabolism and thermoregulation of individual smaller than L. cinereus (Smith et al. 2003) and therefore and clustered long-fingered bats, Miniopterus schreibersii, and gain even larger energy savings from torpor. Moreover, the implications for roosting. S Afr J Zool 34:166–172 short torpor bouts during part of the roost day are likely Chruszcz BJ, Barclay RMR (2002) Thermoregulatory ecology of a to have minimal impact on the duration of pregnancy or solitary bat, Myotis evotis, roosting in rock crevices. Funct Ecol 16:18–26 on daily milk production. Thus, the ability to enter Cryan PM, Wolf BO (2003) Sex differences in the thermoregulation torpor at low Ta could provide energy savings that result and evaporative water loss of a heterothermic bat, Lasiurus in an overall increase in the fitness of reproductive bats. cinereus, during its spring migration. J Exp Biol 206:3381–3390 Our experimental results support field observations Dwyer PD, Harris JA (1972) Behavioural acclimatization to tem- that patterns of torpor use in summer reflect differences perature by pregnant Miniopterus (Chiroptera). 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