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First published online November 28, 2008
Journal of Experimental Biology 211, 3871-3878 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.023101
Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of lesser long-eared bats
Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, New South Wales, 2351 Australia
Author for correspondence (e-mail:
cturbill{at}une.edu.au)
Accepted 23 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: arousal, bat, daily energy expenditure, passive rewarming, temperature, torpor
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). During
torpor, metabolic rate (MR) is greatly reduced because of the suspension of
thermoregulatory heat production at an ambient temperature
(Ta) above the critical minimum in torpor, lowered body
temperature (Tb) and, at least in some heterothermic
mammals, biochemical depression of metabolic activity
(Hock, 1951;
Song et al., 1997;
Storey and Storey, 1990;
Heldmaier and Ruf, 1992;
Geiser, 2004). Although
rewarming of Tb during arousal requires an enormous
increase in MR, even very brief torpor bouts can provide energy savings to
small animals (Tucker, 1962;
Hiebert, 1990;
Cryan and Wolf, 2003). The
major drawbacks of using torpor appear to be the possible negative effect of
low Tb and depressed MR on biochemical and physiological
processes, cognition and behaviours that are likely to be beneficial during
normothermia (van Breukelen and Martin,
2002a; Carey et al.,
2003). The use and daily timing of torpor should therefore reflect
a trade-off between the benefits of elevated Tb and MR
during normothermia and the associated energy costs of thermoregulatory heat
production.
Thermal energetics typically are studied in the laboratory at constant
Ta to derive species-specific values of basal, resting and
torpid MR. In wild animals, however, behavioural decisions will greatly affect
thermoregulatory energy costs during resting. For example, small animals can
select among a wide range of thermal microclimates available in terrestrial
environments (Wolf and Walsberg,
1996; Kerth et al.,
2001; Willis and Brigham,
2005). Moreover, even small differences in use and timing of
torpor versus normothermia in response to thermal conditions within
shelters will have a large impact on resting energy expenditure
(Willis et al., 2004). Season,
body fat reserves, food availability and ambient temperature
(Ta) are all known to influence an animal's propensity to
use torpor (Geiser, 2004). The
circadian timing of torpor entry and arousal is also well known
(Willis, 1982;
Körtner and Geiser,
2000), but the application of these studies to wild populations is
often limited by the use of a constant Ta generally
employed in the laboratory. Whereas, many animals experience a daily
Ta cycle in their resting shelter and this appears to be
an important cue for the timing of torpor and arousal
(Körtner and Geiser,
2000; Mzilikazi et al.,
2002; Turbill et al.,
2003a). In general, small nocturnal mammals show a high propensity
for torpor in the early morning, when daily Ta are
minimal, and arouse at around midday or in the early afternoon, seemingly in
response to a rising Ta in their shelter and some passive
rewarming of torpid Tb
(Davis and Reite, 1967;
Schmid, 1996;
Körtner and Geiser, 2000;
Geiser et al., 2004;
Körtner et al., 2008).
Captive animals typically arouse several hours before their nocturnal active
phase even under constant Ta and it is suggested that this
timing may reflect an inherent propensity for arousal coinciding with rising
Ta and passive rewarming in the wild
(Körtner and Geiser,
2000). Nevertheless, no previous studies have clearly separated
the effects of a daily Ta cycle from the influence of
endogenous circadian cues and the photoperiod on timing of torpor and arousal
patterns.
The present study aims to quantify how a temporal shift in an identical
daily Ta cycle affects Tb cycles and
thermal energetics of male lesser long-eared bats (Nyctophilus
geoffroyi Leach 1982). In the wild, male N. geoffroyi typically
roost solitarily under exfoliated bark of trees and torpor patterns closely
reflect the external daily Ta cycle
(Turbill et al., 2003a).
However, when these bats occasionally use well-insulated tree roosts, in which
daily Ta cycles are reduced in amplitude and delayed,
arousals occur later in the day and after less passive rewarming. These
observations suggest that the timing and extent of diurnal heating interact in
triggering arousals. To distinguish the effects of Ta and
time of day on the temporal organisation of heterothermy, we exposed captive
bats to a diurnal Ta profile that matched natural roost
conditions, but shifted the timing of the daily heating and cooling phases. We
tested the hypothesis that small heterothermic bats arouse from torpor at a
critical threshold of rising Ta and passive rewarming of
torpid Tb, reflecting a trade-off between their high
thermoregulatory costs and the requirements for physiological processes only
possible at normothermic Tb and MR. If so, the timing of
torpor and normothermic periods will be independent of time of the day and
instead closely reflect the timing of the daily Ta cycle.
Alternatively, there may be an interaction between the effects of rising
Ta and time of the day on the critical
Ta for arousal, as suggested by field data. Furthermore,
we aimed to quantify the energetic savings gained by timing arousals and
normothermic periods to coincide with passive rewarming and maximum daily
Ta while day-roosting.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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10 km away) where metabolic measurements commenced on the
night of capture or occasionally on the following afternoon. Measurements for
each bat continued over the next 4 days, after which bats were released at the
capture site. Each day, bats were removed from respirometry chambers for
approximately 1 h after lights-off and following arousal from torpor. During
this time, they were weighed, provided with water and hand fed 1.0±0.3
g of mealworms, and weighed again before being returned to their respirometry
chamber. Bats remained within 0.5 g of capture body mass while in
captivity. Each bat was exposed to each of three daily Ta patterns, which were identical in profile but temporally shifted so that the heating phase commenced at 06:00 h, 09:00 h or 12:00 h (Fig. 1). Over the first 3 days, the sequence of time of heating was chosen randomly. To test for possible effects of time in captivity, the timing of the Ta profile experienced by each bat on day 1 was repeated on day 4. We found no significant effect of time in captivity on the thermoregulatory response of bats (paired t-tests: P>0.05). Bats were exposed to a dim incandescent light from 06:00 h to 18:15 h to mimic the natural photoperiod at that time of the year.
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). A minimum Ta of 12.8±0.9°C
(±s.d.) was maintained throughout the night and heating commenced the
following day at 06:00 h, 09:00 h or 12:00 h
(Fig. 1) and lasted for 4 h 40
min at a rate of 0.05°C min–1 until
Ta reached a maximum 26.6±0.8°C. A plateau of
maximum Ta was maintained for 2 h, before cooling
commenced at an identical rate until the minimum Ta was
reached or, when heating had commenced at 12:00 h, the end of measurements for
that day (i.e. following lights-off and arousal).
Temperature telemetry
Prior to metabolic measurements, a temperature-sensitive radio-transmitter
(Titley Electronics, Ballina, Australia; model LT1, 0.45 g) was attached to
each bat to measure its skin temperature (Tskin). For
small bats, Tskin is closely related to
Tb, particularly during torpor when
Tb–Ta differentials are usually
1–2°C (Audet and Thomas,
1996; Barclay et al.,
1996; Willis and Brigham,
2003). Each transmitter was calibrated against a precision mercury
thermometer (±0.1°C) in a water bath prior to use and attached,
after removing a small patch of hair, to the mid-dorsal skin of the bat using
a rubber-based adhesive (Skinbond; Smith and Nephew, Mt Waverley, Victoria,
Australia). Transmitters were removed from bats at the end of the 4-day
measurement period using an alcohol based removal agent (Universal Adhesive
Remover; Smith and Nephew). The Tskin of bats in
respirometry chambers was measured (via inter-pulse interval) every 3
or 4 min using an FM receiver (Yaesu, F-9600; Cypress, CA, USA) connected
via an A/D converter to a computer or a datalogger (for details, see
Körtner et al., 1998).
Metabolic measurements
Bats were weighed (±0.1 g) immediately prior to measurements and, on
subsequent days, immediately after they were removed from respirometry
chambers in the early evening (before feeding) and again prior to being
re-introduced into the chambers. A linear rate of mass loss was assumed over
each day to calculate mass-specific MR values. Respirometry chambers were made
from cylindrical, clear Perspex tubes (volume: 0.140 l) lined internally with
plastic mesh and hung vertically inside the temperature-controlled cabinet.
Air flow (75–300 ml min–1) was controlled with
rotameters and measured using mass flowmeters (Omega FMA-5606; Stamford, CT,
USA). A lower flow rate (75–100 ml min–1) allowed
greater accuracy of measurements while bats were in torpor.
Ta inside the chambers was measured (±0.1°C) by
a thermocouple inserted 5 mm into the chamber. Flow rate and
Ta were digitized using a 14-bit A/D converter card and
captured using a datalogger (Datataker DT 100F, Data Electronics) before being
recorded by computer software, which was written by G.K., B. Lovegrove and T.
Ruf.
The percentage oxygen differentials of a sub-sample (flow rate: 50 ml
min–1) of air from the respirometry chambers and a reference
channel (outside air) were measured using either an Ametek Applied
Electrochemistry S-3A/II analyser (Naperville, IL, USA; in 2003) or a Sable
Systems FC-1B analyser (Sable Systems International, Las Vegas, NV, USA; in
2004;). Measurements did not differ between analyser systems under similar
thermal conditions (t-tests, P>0.05). The Ametek S-3A/II
was a dual system that enabled measurement of two bats in parallel every 3
min, interrupted by switching to a reference channel every 12 min. The set-up
using the Sable Systems analyser switched in series every 3 min between two
bats and a reference channel, providing a measurement per bat every 9 min.
Switching between channels was controlled using solenoid values. The outputs
from the Ametek analyser, after conversion via a 14-bit A/D card, and
the digital output from the Sable Systems analyser, were recorded using
data-acquisition software onto a personal computer. Rates of oxygen
consumption were calculated using STPD volumes from equation 3a of Withers
(Withers, 1977) and a
respiratory quotient (RQ) of 0.85 was assumed throughout. All equipment was
calibrated prior to use.
Data analysis
Torpor entry was defined as the pronounced decline in MR below the mean
basal MR minus 1 s.d. published for N. geoffroyi
(Geiser and Brigham, 2000).
Periods of passive rewarming were characterised by a slow increase in
Tskin, in parallel to Ta, that were
accompanied by a gradual increase in average MR. Arousals were clearly defined
by a rapid increase in MR to a maximum peak (overshoot) usually followed by a
decrease to resting values, and a concurrent rise in Tskin
to normothermic levels. Arousal was assumed to last until the last measurement
prior to MR having decreased to less than 75% of maximum peak MR or, for
occasional cases where peak MR was followed by sustained high values owing to
activity, to the last measurement of MR that occurred after
Tskin reached 30°C. MR was averaged over this period
and multiplied by the duration of arousal to calculate total energy
expenditure for each arousal. Energy expenditure (kJ) was calculated from
oxygen consumption (ml O2 g–1) using a conversion
factor of 20.083 (Schmidt-Nielsen,
1997).
Average mass-specific MR of resting normothermic bats was calculated over >30 min at minimum and maximum Ta. During passive rewarming of torpid bats, average MR was calculated over the duration of 2°C intervals in heating of Ta (also >30 min). Rest phase energy expenditure was calculated by integrating measurements between the times of lights on and off, or until bats had aroused from torpor, which sometimes occurred shortly after lights off. This was considered to be a realistic definition because it is necessary for bats to regain normothermy prior to their normal active phase and emergence from the roost.
Statistical tests were conducted using Minitab Statistical Software V13.1. Null hypotheses were rejected at P<0.05. Values are presented as means ± 1 s.d. Repeated measures ANOVA (RM ANOVA) was used to compare response variables among treatment days (commencement of heating at 06:00 h, 09:00 h or 12:00 h) within individual bats. To avoid pseudo-replication, mean values were calculated from number of individuals (n) rather than observations (N). General linear modelling (GLM) was used to analyse the relationship between dependent and independent variables. Regression coefficients and r2 values were derived from the fitted model for groups that differed significantly.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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A period of normothermia coincided with the plateau of maximum Ta. On days when heating commenced at 12:00 h, Ta remained at the daily maximum and bats remained normothermic until lights off (Fig. 1, Fig. 2C). On days when heating commenced at 06:00 or 09:00 h, bats re-entered torpor in response to subsequent cooling of Ta, even late in the afternoon, before always arousing again close to the time of lights off (Fig. 1, Fig. 3A,B). Bats re-entered torpor during cooling at a Ta of 24.9±2.8°C and 22.8±2.7°C on days when heating commenced at 06:00 h and 09:00 h, respectively, which did not differ significantly (RM ANOVA: F1,13=2.2, P=0.16).
Normothermic periods lasted longer on days when heating commenced at 09:00 h (3:42±1:26 h), owing to the lower Ta at arousal and torpor re-entry, than on days when heating had commenced at 06:00 (2:01±1:33 h) or 12:00 h (2:50±1:08 h; repeated ANOVA: F2,32=6.1, P<0.01; Tukey's test: 09:00 vs 06:00 h or 12:00 h, P<0.05). The duration of normothermic periods was cut short on days when heating had commenced at 12:00 h by the time of lights-off and beginning of the active phase.
During passive rewarming of bats in torpor, mass-specific MR increased exponentially from an average of 0.06±0.02 ml O2 g–1 h–1 at Ta of 10–12°C (Tskin 11–13°C) to 0.53±0.12 ml O2 g–1 h–1 at Ta of 26–28°C (Tskin 26–29°C) (Fig. 4) [Torpid MR (ml O2 g–1 h–1)= 0.015x1.141Ta (r2=0.78, P<0.001)]. During periods of normothermy, average mass-specific resting MR was 7.0±0.7 ml O2 g–1 h–1 at a minimum Ta of 13.7±0.7°C and was reduced to 3.0±0.6 ml O2 g–1 h–1 at a maximum Ta of 26.5±0.7°C.
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Energy expenditure of bats over the entire rest phase (12 h) increased linearly depending on the time spent normothermic (Fig. 6), ranging from a minimum of 0.59 kJ for a bat remaining torpid throughout the day to a maximum of 3.60 kJ for a bat that was normothermic for 5:06 h (mean: 1.98±0.84 kJ). The slope of the relationship between rest phase energy expenditure and time spent normothermic did not differ significantly among the different thermal regimes (GLM: slope, F2,41=2.4, P=0.1). However, the amount of energy expended for a given time period spent normothermic was significantly greater for bats on days when heating commenced at 06:00 h and 09:00 h in comparison to 12:00 h (GLM: y-intercept, F1,43=287.1, P<0.001; Tukey's test: 12:00 h vs 06:00 h or 09:00 h, P<0.001). The additional energy expenditure of bats on days when heating commenced at 06:00 h and 09:00 h resulted from the need for a second, completely active arousal near lights off prior to the active phase. The average cost of the second arousal near lights off was significantly greater for bats on days when heating commenced at 06:00 h (0.46±0.09 kJ) than at 09:00 h (0.31±0.12 kJ; RM ANOVA: F1,15=35.2, P<0.001) because of the greater cooling of Ta and Tb of torpid bats prior to active arousal on these days.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Captive bats were torpid in the morning coinciding with daily
Ta minima and aroused after reaching a threshold level of
passive rewarming from rising Ta during the day.
Importantly, this critical arousal Ta is not a fixed
parameter, but depends on the time of day. Bats synchronised a period of
normothermy with the time of the daily plateau of Ta
maxima and re-entered torpor in response to cooling of Ta
in the afternoon. Selection of poorly insulated rest sites is not uncommon
among bats and appears particularly common in solitary roosting males
(Kurta and Kunz, 1988;
Kurta et al., 1989;
Bronner et al., 1999;
Chruszcz and Barclay, 2002;
Kunz and Lumsden, 2003;
Lausen and Barclay, 2003;
Turbill et al., 2003b;
Turbill, 2006a;
Turbill, 2006b). A number of
heterothermic mammals also prefer rest sites that receive direct solar
radiation, which increases the amplitude of heating of shelter
Ta during the day
(Vaughan and O'Shea, 1976;
Humphrey et al., 1977;
Hosken, 1996;
Kerth et al., 2001;
Geiser et al., 2002;
Mzilikazi et al., 2002;
Mzilikazi and Lovegrove,
2004). By co-ordinating torpor and normothermy with the daily
Ta cycle, small species like N. geoffroyi can
exploit the high Ta provided in thermally unstable roosts
to minimise the energetic cost of arousal and a period of normothermy during
the rest phase.
The energy expenditure of torpid bats remained a small fraction of
normothermic costs even during exposure to a wide daily fluctuation in
Ta. Metabolic rate of torpid bats at the maximum
Ta of 27°C, when Tskin was
passively rewarmed to around 28°C, remained only 15% of normothermic
values at the same Ta and 39% of BMR
(Geiser and Brigham, 2000).
Moreover, if torpid MR is extrapolated to Ta of
29.1°C, the lower limit of the thermal neutral zone (TNZ) in N.
geoffroyi, the predicted torpid MR remains only 50% of BMR
(Fig. 4). Our experimental
design, where torpid animals were slowly warmed to near their TNZ, provides
unique support for temperature-independent mechanisms of metabolic depression
in small hibernators (Geiser,
1988; Song et al.,
1997; Buck and Barnes,
2000; Geiser and Brigham,
2000). Superficially, it could appear that the reduced
Tb–Ta differential during torpor
(2°C) compared with during normothermia (5°C) actually
caused the much lower torpid metabolic rate (TMR) relative to BMR at a
Ta in the TNZ. However, the lower
Tb–Ta differential is clearly a
result, not the cause, of the lower TMR
(Geiser, 2004). Because the
thermal conductance of torpid N. geoffroyi at a
Ta near the TNZ is similar to that during normothermia
(Geiser and Brigham, 2000),
the 5°C lower Tb of torpid bats reflects their
reduced heat production at a lower TMR, not the other way around. This is an
important point because it shows, firstly, that the energy savings to costs of
arousal from passive rewarming are even greater than they would be if TMR was
solely a function of temperature, and, secondly, that the energy savings if
the bats remain in torpor are relatively little affected by the wide daily
Ta variations in their poorly insulated tree roosts.
Although torpid MR remained much below BMR during heating, the exponential
relationship with Ta resulted in a greater rate of
increase in MR as Ta approached the TNZ. Expressed as a
proportion of BMR, TMR increased by 6.6% over 5°C with warming of
Ta from 15°C to 20°C, but increased by 12.8% with
warming of Ta from 20°C to 25°C. Active arousals
were more common after heating of Ta above 20°C,
suggesting that increased MR may play a role in stimulating arousals in
response to passive rewarming (Schmid,
1996). This Tb threshold may also reflect a
transition to greater levels of translation and protein synthesis
(van Breukelen and Martin,
2001) and activity of the brain and central nervous system during
torpor (Carey et al., 2003),
which could lead to a greater propensity for active arousal.
Laboratory studies under constant Ta have found that
whereas times of entry into torpor are variable and occur earlier in the
active phase under conditions of energetic stress, times of arousal appear
largely fixed according to an endogenous circadian rhythm
(Tucker, 1962;
Brown and Bartholomew, 1969;
Geiser, 1986). By contrast, in
wild animals, times of arousal frequently coincide with an initial period of
passive rewarming during the day (Geiser
et al., 2004), suggesting that these arousals are triggered by a
threshold level of exogenous rewarming
(Schmid, 1996;
Lovegrove et al., 1999;
Körtner and Geiser,
2000). Our experiment has shown, by manipulating the timing of
diurnal heating relative to the photophase, that arousals in a small bat are
not fixed, but triggered to occur during the day according to the timing of
passive rewarming from rising Ta, in addition to the
strong arousal cue from the photoperiod.
The interaction between Ta and time of the day as a cue
for arousal can be represented in a simple model
(Fig. 7). This model suggests
that arousals are triggered if and when Ta reaches a
curvilinear threshold. Furthermore, the model suggests that at
Ta below the lower asymptote of the arousal threshold,
such as when roosting in cool caves, bats should remain in torpor until dusk.
This is the daily pattern observed in captive N. geoffroyi under
constant cool temperatures (Geiser and
Brigham, 2000). Remaining in torpor early in the morning provides
maximum energy savings when daily Ta is typically minimal.
The progressive sensitivity of N. geoffroyi to a thermal arousal cue
over the course of their rest phase somewhat resembles that found in
hibernating ground squirrels over multiday bouts of torpor (Bechman and
Stanton, 1978). Similarly, it may indicate an increase in the sensitivity of
the bat's central nervous system over the course of the torpor bout, perhaps
reflecting an expectation of the strong circadian cue for arousal at dusk.
Alternatively, from a behavioural perspective, as the time available for a
normothermic period during the rest phase diminishes, N. geoffroyi
may arouse at lower Ta despite the higher cost for arousal
and normothermy. Surprisingly, the increasing predisposition for arousal did
not reflect an inclination to remain normothermic later in the rest phase, as
N. geoffroyi always re-entered torpor in response to a decrease in
Ta, despite the need for a second arousal shortly after at
dusk. Hence, the timing of normothermic periods was finely tuned to short-term
fluctuations in Ta that affected thermoregulatory costs
during the rest phase.
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The fact that bats aroused well before the beginning of their active phase,
whereas, to maximise their energy savings, they could have remained torpid,
indicates that some period of normothermia is advantageous prior to the active
phase. Their behaviour suggests that, above a threshold
Ta, the benefits of normothermia outweigh the
thermoregulatory energy cost. Bats were usually motionless in the respirometry
chambers during midday bouts of normothermia, possibly indicating these
periods were important for physiological rather than behavioural reasons. For
wild bats, the risk of predation while roosting under tree bark is likely
greatest in the early morning when large diurnal birds that search under bark
for arthropods are most active, but bats show a strong tendency for torpor at
this time. The short duration of many normothermic bouts and their close
synchrony with maximal Ta in captive and wild bats also
suggests that alertness to predators is not a primary reason for arousing. The
most parsimonious explanation for the apparent preference for normothermia
during resting in long-eared bats is to facilitate the numerous biochemical
and physiological processes that are retarded by a low Tb
and MR during torpor bouts. For example, bats may arouse to allow for
restorative sleep processes, protein synthesis or even the digestion of food
captured the previous night (Storey and
Storey, 1990; Daan et al.,
1991; van Breukelen and
Martin, 2002b).
By co-ordinating torpor, arousal and normothermy with short-term changes in
Ta, small bats appear to gain an energetic advantage from
selecting roosts containing a wide daily Ta cycle. Energy
costs at low Ta in the early morning are avoided by using
torpor, whereas passive rewarming from diurnal heating provides largely
reduced energetic cost of rewarming from torpor. However, the energy savings
gained from passive rewarming are not as significant for small heterotherms,
such as N. geoffroyi, as they are for larger species
(Lovegrove et al., 1999). Much
greater energy savings are gained from the reduction in subsequent
thermoregulatory costs. For example, whereas the cost of arousal of N.
geoffroyi at Ta of 13°C was 0.5 kJ, the cost
of a subsequent 3 h normothermic period is reduced by 1.7 kJ at a
Ta of 27°C rather than 13°C. The minor cost of
arousal relative to continuous normothermic thermoregulation, even at mild
Ta, promotes a highly dynamic pattern of torpor in these
bats, which is remarkably similar to the opportunistic endothermy of bees and
moths (Heinrich, 1974). The
low rewarming costs are an important advantage of a small body size in a
heterothermic endotherm. Moreover, frequent shifting between physiological
states allows these bats to exploit thermally unstable day-roosts, which,
although cold in the morning, provide a short period of high daily
Ta maxima during the day.
Behavioural decisions greatly influence the resting energy expenditure of
small heterothermic mammals such as bats. Shelter microclimate, in particular,
can determine the timing and energy costs of thermoregulatory behaviour.
Moreover, even within an identical thermal regime, variation in duration of
torpor versus normothermia by N. geoffroyi resulted in a
fivefold difference in rest-phase energy expenditure. Although
species-specific values of resting and torpid MR are easily measured and
available for many species (Speakman and
Thomas, 2003), the extent by which they affect daily energy
expenditure is easily outweighed by variation among and within species in
their choice of shelter microclimate and heterothermic behaviour. This fact
cautions against a straight forward energetic interpretation of these values,
especially for small heterothermic endotherms. An analysis that incorporates
the potentially large effect of behavioural decisions would provide a more
accurate picture of their physiological adaptations to manage a limited energy
budget.
LIST OF ABBREVIATIONS
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Daan, S., Barnes, B. M. and Strijkstra, A. M. (1991). Warming up for sleep? Ground squirrels sleep during arousals from hibernation. Neurosci. Lett. 128,265 -268.[CrossRef][Medline]
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