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 Ó 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)of15°C. 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±1.1°C 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 1–2°CofTa over a wide shows that under identical thermal conditions, thermal range of Ta above the Tb set-point (2°C 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 15°C 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 >10°C) 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±1.1°C 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 20°C 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 (30°35¢S, 2003a), whereas reproductive female bats congregate in 151°41¢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 10°C 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 9.8°C and a maximum of Hall 1982). Furthermore, females and their young in 24.3°C 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 (±0.1°C) 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.