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Torpor, Thermal Biology, and Energetics in Australian Long-Eared Bats (Nyctophilus)

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Torpor, Thermal Biology, and Energetics in Australian Long-Eared Bats (Nyctophilus) J Comp Physiol B (2000) 170: 153±162 Ó Springer-Verlag 2000 ORIGINAL PAPER F. Geiser á R. M. Brigham Torpor, thermal biology, and energetics in Australian long-eared bats (Nyctophilus) Accepted: 22 November 1999 Abstract Previous studies have suggested that Austra- had torpor metabolic rates that were up to ten times lian long-eared bats (Nyctophilus) dier from northern- higher than those measured overnight. The steady-state hemisphere bats with respect to their thermal physiology torpor metabolic rate of thermoconforming torpid bats and patterns of torpor. To determine whether this is a showed an exponential relationship with body temper- general trait of Australian bats, we characterised the ature (r2 = 0.94), suggesting that temperature eects are temporal organisation of torpor and quanti®ed meta- important for reduction of metabolic rate below basal bolic rates and body temperatures of normothermic and levels. However, the 75% reduction of metabolic rate torpid Australian bats (Nyctophilus georoyi, 7 g and between basal metabolic rate and torpor metabolic rate N. gouldi, 10 g) over a range of air temperatures and in at a body temperature of 29.3 °C suggests that metabolic dierent seasons. The basal metabolic rate of normo- inhibition also plays an important role. Torpor meta- thermic bats was 1.36 0.17 ml g)1 h)1 (N. georoyi) bolic rate showed little or no seasonal change. Our study and 1.22 0.13 ml g)1 h)1 (N. gouldi), about 65% of suggests that Australian Nyctophilus bats have a low that predicted by allometric equations, and the corre- basal metabolic rate and that their patterns of torpor are sponding body temperature was about 36 °C. Below an similar to those measured in bats from the northern air temperature of about 25 °C bats usually remained hemisphere. The low basal metabolic rate and the high normothermic for only brief periods and typically en- proclivity of these bats for using torpor suggest that they tered torpor. Arousal from torpor usually occurred are constrained by limited energy availability and that shortly after the beginning of the dark phase and torpor heterothermy plays a key role in their natural biology. re-entry occurred almost always during the dark phase after normothermic periods of only 111 48 min Key words Bats á Body temperature á Metabolic (N. georoyi) and 115 66 min (N. gouldi). At air rate á Nyctophilus á Torpor bouts temperatures below 10 °C, bats remained torpid for more than 1 day. Bats that were measured overnight had Abbreviations BMR basal metabolic rate á C thermal steady-state torpor metabolic rates representing only conductance á MR metabolic rate á RMR resting 2.7% (N. georoyi) and 4.2% (N. gouldi) of the basal metabolic rate á Ta air temperature á Tb body metabolic rate, and their body temperatures fell to temperature á TMR torpor metabolic rate á TNZ _ minima of 1.4 and 2.3 °C, respectively. In contrast, bats thermoneutral zone á V O2 rate of oxygen consumption measured entirely during the day, as in previous studies, Introduction Communicated by I.D. Hume With the exception of rodents, bats are the only non- marine placental mammals endemic to Australia. It is F. Geiser (&) believed that the ®rst bats migrated to Australia from Zoology, School of Biological Sciences, south-eastern Asia in the mid Tertiary and evolved into University of New England, Armidale NSW 2351, Australia several distinct Australian genera (Hall 1984). Despite e-mail: [email protected] this evolutionary background and the long separation Fax: +61-2-67-733-814 from bats in other parts of the world, little detailed work has been conducted to determine whether physiological R. M. Brigham Department of Biology, University of Regina, adaptations of Australian bats dier from those found Regina, Saskatchewan, Canada on other continents. It is possible that the aridity, 154 unpredictable rainfall, and infertile soils characteristic of undergo short torpor bouts usually lasting for less than a the Australian continent are re¯ected in energetic and day in summer, and multi-day torpor bouts (i.e. hiber- thermoregulatory features of bats as have been observed nation) in winter (Hall 1982; Ellis et al. 1991; Brigham in marsupials (Dawson 1989; Lovegrove 1996). It is and Geiser 1998; Turbill et al. 1999) similar to northern- known that Australian microbats (Microchiroptera) as hemisphere species (Audet and Fenton 1988). As torpor well as small megabats (Megachiroptera) use torpor bout duration in many heterothermic mammals appears extensively to reduce energy expenditure (Morrison to be related to Tb and MR (Twente and Twente 1965; 1959; Kulzer et al. 1970; Morris et al. 1994; Geiser et al. French 1985; Geiser and Kenagy 1988; Barnes and 1996; Hosken 1997; Bartels et al. 1998; Coburn and Ritter 1993), it is possible that bats either change the- Geiser 1998; Hosken and Withers 1999). This is most rmoenergetics with season, or that bout duration is to a likely because of their large relative surface area, high large extent controlled by external factors such as Ta and costs for thermoregulation at low air temperature (Ta), food availability. To our knowledge there is no pub- and unpredictable or temperature-dependent food sup- lished literature on whether the seasonal change in tor- ply as in bats from Europe and North America (Hock por bout duration of bats in general re¯ects seasonal 1951; Pohl 1961; Henshaw 1970; Lyman 1970; Kunz changes in MR during torpor. 1982; Fenton 1983; Thomas et al. 1990; Speakman et al. We quanti®ed patterns of thermoregulation, ener- 1991; Barclay et al. 1996). getics, and the duration of normothermic periods and Some recent studies on endemic Australian long- torpor bouts in two species of long-eared bats, N. eared bats of the genus Nyctophilus (Family Vespertili- georoyi and N. gouldi, to determine whether they onidae) suggest that they may dier considerably from dier from northern-hemisphere bats. We measured northern-hemisphere species with respect to the physi- the MR of bats overnight to allow them to enter ology of torpor. Body temperature (Tb), metabolic rate torpor during the night or near sunrise as in the ®eld, (MR), and the dierential between Tb and Ta reported in and assessed whether these values diered from those several species of these tree-cavity roosting bats (Ny- obtained from bats measured entirely during daytime. ctophilus georoyi, N. gouldi and N. major) during tor- Further, we investigated interrelations between physi- por are relatively high (Morris et al. 1994; Hosken 1997; ological variables associated with torpor and deter- Hosken and Withers 1999). Whereas the Tb of many mined whether MR during torpor (TMR) diers torpid vespertilionids from the northern hemisphere fall among seasons. to near 0 °C, and the dierential between Tb and Ta is often around 1 °C (Hock 1951; Henshaw 1970; Lyman 1970; Geiser and Ruf 1995), torpid Australian long- Materials and methods eared bats appear to maintain a Tb of >10 °C, and a Tb±Ta dierential that is more than twofold, and a MR Bats were captured in mist nests in Imbota Nature Reserve (for- that is up to tenfold that of northern-hemisphere ves- merly Eastwood State Forest) near Armidale, New South Wales pertilionids. Some of these dierences may be due to (30°35¢S, 151°44¢E), an open woodland area at approximately 1000 m altitude. Captured animals were transferred to the labo- climatic factors; however, eects of captivity or experi- ratory at the University of New England and measured over a mental conditions may also play an important role period of 1±3 days before being released at the site of capture. To (Hosken 1997; Hosken and Withers 1999). With respect ensure that bats held for more than 1 day maintained condition to experimental conditions it may be important that all while in captivity, they were hand fed with mealworms and water once per day while not being measured. Measurements were recently published experiments used to quantify physi- conducted on a total of 24 N. georoyi (September 1996 to May ological variables of torpid Australian long-eared bats 1997) and 9 N. gouldi (January to July 1997). _ (Nyctophilus spp.) were conducted with individuals in The MR, measured as rate of oxygen consumption (VO2), was which torpor was induced during the day and measured monitored over periods ranging from several hours to several 2±3 h after entry into torpor around the time when free- days over a range of Tas and natural photoperiod. TMR was averaged from minimum measurements that remained constant living Nyctophilus bats typically arouse (Turbill et al. over at least 30 min. Two types of measurements were performed: 1999). In contrast, many measurements on northern- (1) overnight and the following day(s), and (2) entirely during hemisphere bats were conducted overnight to allow daytime. them to undergo their natural thermal cycle with torpor Most bats were measured beginning in the afternoon, overnight and throughout most of the following day to allow them to un- entry at night or around dawn, or bats were transferred dergo their natural daily thermal cycle with torpor entry during the to the measuring equipment while hibernating night or near sunrise (Turbill et al. 1999; Figs. 1, 2). Readings were (Hock 1951; Pohl 1961; Henshaw 1968; Riedesel and taken in the morning after torpor bouts of at least 4 h (average Williams 1976; Thomas et al. 1990; Speakman et al. 10.5 h) at the time when bats are naturally torpid (Turbill et al. 1999). Initially, we followed the protocol of Hosken (1997) and 1991). Riedesel and Williams (1976) showed that the other recent studies of Nyctophilus spp., beginning measurements in time to reach minimum MR during torpor in Myotis mid-morning, and taking readings after bats were in torpor for 2± velifer (12 g) was up to 19 h from the beginning of 3 h.
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