Sex differences in the thermoregulation and evaporative water loss of a heterothermic bat, Lasiurus cinereus, during its spring migration
UNM Department of Biology, MCS03 2020, 1 University of New Mexico, Albuquerque, New Mexico 87131-0001 USA
* Author for correspondence (e-mail: paulcryan{at}lycos.com)
Accepted 27 June 2003
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Summary |
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Key words: Chiroptera, thermoregulation, energetics, body temperature, metabolic rate, conductance, evaporative water loss, torpor, sex difference, hoary bat, Lasiurus cinereus
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Introduction |
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Within a given species, however, torpor may not benefit each sex to the
same degree. Differences are likely to be particularly pronounced during the
periods when females are pregnant or lactating. Insectivorous bats produce
offspring that exhibit some of the slowest rates of fetal development, and
relatively longest periods of postpartum dependence known among
mammals (Eisenberg, 1981;
Hayssen, 1993
;
Kunz and Stern, 1995
). Once
weaned, juvenile bats must also learn to forage efficiently, and accumulate
adequate energy stores before environmental conditions become unfavorable and
prompt either migration or hibernation. For temperate species, these
activities must occur within a relatively short period of time when climate
and resource availability are amenable to successful reproduction. Fetal
development and postpartum growth in bats are temperature-dependent
processes that cooler temperatures generally retard
(Kunz and Stern, 1995
;
Racey, 1973
;
Racey and Swift, 1981
).
Although torpor can ameliorate both energy and water demands in reproductive
females (Wilde et al., 1999
),
the associated low body temperatures would lengthen developmental periods and
potentially lead to increased maternal and juvenile mortality
(Kunz and Hood, 2000
).
Male bats face different energy and time constraints compared to
reproductive females (Barclay,
1991). Current evidence indicates that the greatest energy demand
in males coincides with spermatogenesis
(Racey and Entwistle, 2000
)
and, although considerable resources may be diverted toward sperm production,
it is unlikely that reproductive costs for males exceed those of females
(Gittleman and Thompson,
1988
). In addition, the timing of reproductive demands differs
between the sexes. Spermatogenesis in vespertilionids typically occurs in
summer, followed by mating activity during late summer through winter
(Racey and Entwistle, 2000
).
In contrast, for females, the ever-increasing energy demands of pregnancy and
lactation begin in early spring and continue through autumn
(Racey and Speakman, 1987
).
Given the phenological and quantitative differences in energy demands between
male and reproductive female bats during spring, it seems plausible that
differences in their use of torpor occur.
Field studies suggest that male insectivorous bats enter torpor more
frequently than reproductive females
(Kurta and Fujita, 1988). For
instance, male big brown bats Eptesicus fuscus in Canada use torpor
more frequently than reproductive females during summer
(Grinevitch et al., 1995
;
Hamilton and Barclay, 1994
).
In light of such evidence, it has been proposed that males (and
non-reproductive females) use torpor more frequently than reproductive
females, are capable of withstanding more variable climatic conditions and
may, in some cases, actually select roost microclimates that facilitate torpor
(Barclay, 1991
). Inherent in
such hypotheses is the assumption that males and reproductive females are
capable of different physiological responses when exposed to similar
conditions, rather than simply preferentially selecting different
microclimates. Unfortunately, it is impossible to control the conditions to
which bats are exposed in the field, and laboratory studies aimed at
quantifying sex differences in thermoregulation or use of torpor are lacking
(Kurta and Fujita, 1988
).
This study aimed to quantify sex differences in the short-term
thermoregulatory strategies of hoary bats Lasiurus cinereus captured
during their spring migration. In North America, L. cinereus is a
long-distance migrant that winters in California and Mexico then moves into
northern latitudes of the continent during spring and summer
(Cryan, 2003). Pregnant female
L. cinereus precede males north in early spring and move to more
eastern summering grounds, while males occupy mountainous regions of western
North America (Findley and Jones,
1964
). L. cinereus is an ideal species for examining
sexual differences in thermoregulatory behavior for several reasons: (1)
females are pregnant during migration; (2) energetic demands on males during
spring are presumably low and they are not yet sexually active; and (3) the
microclimates of roosts used by L. cinereus (tree-foliage) are
probably little different from the general environment. Here we report
laboratory work that quantifies variation in body temperature
(Tb), metabolic rate (MR), wet thermal conductance
(Cwet), and evaporative water loss (EWL) of both male and
pregnant female L. cinereus over a range of air temperatures
(Ta).
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Materials and methods |
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Physiological measurements
We used flow-through respirometery to determine the MR,
Cwet and EWL of L. cinereus over a range of
Ta values. Metabolic rates were inferred from measurements
of the rate of carbon dioxide production
(CO2). Bats were
placed in 2 l stainless steel metabolic chambers fitted with perches that
allowed them to hang in a normal roosting position. Excreta was trapped under
1 cm of mineral oil placed in the bottom of each chamber to prevent
interference with EWL measurements. Metabolic chambers were situated within a
temperature-controlled cabinet that maintained constant temperatures
(±1°C) over a range of 0-40°C. Internal chamber temperatures
were continuously measured with thermocouples and a digital thermometer (Sable
Systems TC-1000, Las Vegas, NV, USA). Dry, CO2-free air from a
purge gas generator (Whatman FT-IR, Haverhill, MA, USA) was fed through
rotameters (Scientific Model # FL-3402C, accurate to ±2% of full scale;
Omega, Stamford, CA, USA) or mass flow controllers (FMA Model # FLA-A2409,
accurate to ±1%; Omega) before entering metabolic chambers. Flow meters
were calibrated using a soap-bubble flow meter. Air from the purge gas
generator was also directly sampled, and served as a baseline. The flow rate
of the air into chambers ranged between 0.7 and 1.2 l m-1, to
maintain chamber humidities below 1.0 kPa; time to reach 99% chamber
equilibrium ranged from 6.5 to 11.2 min
(Lasiewski et al., 1966
). Up
to four metabolic chambers were used simultaneously and outlet air from the
chambers was routed to a gas multiplexer (Sable Systems Respirometer
Multiplexer V 2.0), which allowed for sequential sampling of individual
chambers with the gas analyzer. During runs with more than one bat, each
metabolic chamber was sampled for 7.7 min before the multiplexer switched to
the next chamber. Chamber outlet air was monitored with a
CO2/H20 analyzer (Li-Cor LI-7000, Lincoln, NE, USA) and
the digital output from the gas analyzer was sampled 9 times per second by a
computer using DATACAN V data-acquisition software (Sable Systems). The gas
analyzer was calibrated daily using CO2-free air and a reference
gas of 1020 p.p.m. CO2 for CO2 calibration, while dry
air and a dew point generator (LiCor Li-610) were used for water calibration.
Accuracy of CO2 and water channels of the LI-7000 were ±1
p.p.m. and ±0.01 kPa, respectively. All measurements were corrected to
standard temperature and pressure (STP).
Most bats were run only once and at a single temperature, but 17 individuals were run twice at two temperatures with at least 2 h between runs; we did not detect differences in the measured parameters between individuals subjected to a second run and other bats. Experimental runs occurred at 5° increments from 0 to 40°C, and also at 32.5 and 37.5°C. With the exception of runs at 37.5 and 40°C (which lasted only 30-45 min), bats were acclimated to metabolic chambers for 1 h before measurements began. Bat activity was monitored visually and individuals that were not resting quietly after 30 min were excluded from measurements. Experimental runs lasted 1-3 h, during which time carbon dioxide and water readings typically reached stable levels for >10 min. All reported MR and EWL values are averages taken from 1 min of the lowest stable values.
In addition to CO2 and evaporative water loss measurements, we
recorded body temperature (Tb) to ±0.1°C within
15 s of removal from the chambers by inserting a lubricated Teflon coated
copper-constantan thermocouple (Physitemp # NJ07013, Clifton, NJ, USA) 1 cm
into the rectum. Animals were classified as torpid when exit
Tb <30°C; in three instances,
CO2 readings
indicated that bats were using torpor, but Tb indicated a
return to a normothermic state before the end of the run. Therefore, despite
their normothermic exit Tb values, these bats were
considered torpid for subsequent analyses of MR, EWL and
Cwet, but not Tb. Respiratory rates of
several bats were quantified by monitoring pressure fluctuations within the
metabolic chambers using a pressure meter (Sable Systems PT-100B).
Calculation of metabolic rate and minimum wet thermal
conductance
CO2was
calculated as:
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Wet thermal conductance Cwet was calculated using the equation Cwet=MR/(Tb-Ta), where MR is measured in mW g-1 and Tb and Ta are in °C.
Statistical analysis
Statistical analyses were carried out using NCSS 2000 for Windows.
Differences in mean values of variables showing no significant relationship to
Ta were tested using t-tests. Analysis of
covariance (ANCOVA; GLM ANOVA) was used to test for differences in regression
slopes, intercepts and interaction terms between sexes and thermoregulatory
groups (torpor versus normothermia), using sex (or group) as a fixed
effect, and Ta as a covariate. EWL data were linearly
transformed using a natural-log function prior to ANCOVA analysis. We
estimated the thermoneutral zone (TNZ) from values within 1°C of the
Ta values at which actual measurements were made. Reported
values are expressed as means ± standard errors (S.E.M.) and
statistical significance was set at P0.05.
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Results |
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Metabolic rate
As with Tb, metabolic measurements indicated a
dichotomous thermoregulatory response (normothermia and torpor) by bats at
Ta<25°C (Fig.
2). The thermal neutral zone ranged between approximately 30°C
(lower temperature Tlc) and 34°C (upper temperature
Tuc) in both sexes. Within the TNZ, females had
significantly lower mass-specific MR values than males (t=-3.3,
d.f.=13.5, P<0.05), but there were no differences in mass-specific
MR between normothermic males and females below the Tlc
(Ta, F1,49=27.2, P<0.0001;
sex, F1,49=0.2, P=0.69; interaction,
F1,49=1.1, P=0.38). The metabolic rate of males
in torpor was lower and less variable at chamber temperatures between 10 and
20°C (2.1±0.5 mW g-1) than at temperatures between 0 and
5°C (9.8±1.8 mW g-1). At
10°<Ta<15°C, torpor decreased metabolic
expenditure to 4-7% of normothermic values, but the savings of torpor were
generally smaller (22-29% of normothermic values) outside of this temperature
range. We detected no significant differences in the mass (t=1.0,
d.f.=57, P=0.34), forearm length (t=-0.7, d.f.=54,
P=0.46), or amount of guano produced (t=-0.3, d.f.=55,
P=0.75) between heterothermic and normothermic bats.
|
Thermal conductance
Wet thermal conductance increased exponentially above minimum values at
chamber temperatures >30°C in both sexes
(Fig. 3). There was no
significant relationship between Ta and
Cwet below Tlc, nor were there
differences in Cwet between sexes of normothermic bats
(Ta, F1,49=1.1, P=0.36; sex,
F1,49=0.5, P=0.51; interaction,
F1,49=0.7, P=0.60). However,
Cwet values of bats in torpor were significantly lower
than those of normothermic individuals (t=4.2, d.f.=29.6,
P<0.05).
|
Evaporative water loss
Mass-specific rates of EWL were consistently higher in normothermic males
than in females, and increased more rapidly with Ta in
males (Fig. 4;
Ta, F1,99=28.3, P<0.0001;
sex, F1,99=27.4, P<0.05; interaction,
F1,99=3.1, P<0.05). EWL in torpid males was
significantly less than in normothermic individuals at similar
Ta values, but the slopes of the regression lines did not
differ significantly (Ta, F1,27=3.9,
P<0.05; group, F1,27=54.6, P<0.05;
interaction, F1,27=0.1, P=0.99). EWL of bats in
torpor was 63±6% of EWL of normothermic individuals at similar
Ta values.
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Discussion |
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Metabolic rates of normothermic males and females within the TNZ were
106±12% and 74±3%, respectively, of values expected [basal
metabolic rate (BMR)=4.12 m-0.31, where m=body
mass; White and Seymour,
2003]. The MR we observed was higher than that measured by Genoud
(1993
), who found that the BMR
of a single L. cinereus captured during winter and maintained in
captivity was 52% of the expected value
(White and Seymour, 2003
).
Metabolic rates of lasiurines change with season and are generally lower in
winter than during the warmer months (Genoud,
1990
,
1993
), potentially explaining
some of these differences. However, comparisons of data collected from
metabolic studies of bats captured and maintained under different conditions
should be treated with caution (Kurta and
Fujita, 1988
). Unlike males, the mass-specific metabolic rates
measured in females during this study were lower than expected. McLean and
Speakman (2000
) also observed
lower metabolic rates in pregnant bats and suggested that lower metabolic
needs of fetal tissues might contribute to this effect. Increases in the mass
of ametabolic materials during pregnancy may also contribute to the low
mass-specific metabolic rates that we observed in this study. In general,
circulating fluid volume increases with pregnancy in mammals, and the water
content of mammalian embryos is relatively high
(Adolph and Heggeness, 1971
).
Sexual size dimorphism may also influence allometric differences in metabolic
rate. Mass-specific metabolic rate decreases with increasing body size
(White and Seymour, 2003
; but
see Gillooly et al., 2001
) and
L. cinereus is sexually dimorphic, with females averaging 3.9% larger
than males in skeletal measurements
(Williams and Findley, 1979
)
and about 40% larger in mass during pregnancy (this study). Comparative
studies of male and non-reproductive female L. cinereus would help
elucidate whether the lower mass-specific metabolic rates of pregnant females
observed in this study were related to embryonic growth or body size
alone.
Energetic savings associated with the use of torpor
In the hoary bat, as with small mammals in general, the metabolic cost of
maintaining normothermic body temperatures increases rapidly as air
temperatures decrease below the lower critical temperature. Because
maintenance costs in small endotherms comprise a large proportion of total
daily energy expenditure (McNab,
2002), thermoregulation has a considerable influence on overall
energy balance. Metabolic rates of L. cinereus increased sixfold as
chamber air temperature decreased from the 30°C (Tlc)
to 0°C (Fig. 2). Whereas
most males used torpor to reduce thermoregulatory costs, the reluctance of
pregnant females to do so suggests they must have much higher energetic
demands when migrating through cold areas. Indeed, female L. cinereus
routinely encounter sub-thermoneutral environmental temperatures
(<Tlc) during their spring migration, as average air
temperatures within the study area range from 3.4 to 23.4°C during the
months when L. cinereus is found there (Climate Source, Corvalis,
Oregon, USA). At the metabolic rates observed in this study, a roosting 30 g
female L. cinereus would expend approximately 15.6 kJ of energy over
a 24 h period at 30°C and a decrease in environmental temperature to
5°C for the same period would increase total energy expenditure more than
fivefold to approximately 79.0 kJ.These values can be compared to estimates of
field metabolic rate (FMR) in bats using equation 4 of Nagy et al.
(1999
), which predicts an FMR
of 65.8 kJ day-1 (range 25.5-169.6 kJ day-1) for a 30 g
female L. cinereus. In general, these values are consistent with
measured FMR values from other free-ranging insectivorous bats, e.g. pregnant
9 g Myotis lucifugus, 33.7 kJ day-1
(Kurta et al., 1989
); pregnant
18 gEptesicus fuscus, 48.6 kJ day-1
(Kurta et al., 1990
). Given
that the thermoregulatory costs incurred by a normothermic L.
cinereus exposed to low air temperatures could exceed the total daily
energy use of a free-ranging individual, pregnant female L. cinereus
might not maintain a positive energy balance during spring migration through
colder areas, if energy intake were limited (e.g. during inclement
weather).
Males, in contrast, are not constrained physiologically or behaviorally by the needs of the young. As a consequence, males can use torpor to accrue energy or limit foraging. In the laboratory, torpor in males resulted in a reduction in metabolic rate of up to 97% (Ta=0°C, torpor MR=1.1 mW g-1, normothermic MR=40.5 mW g-1).
We can explore the relative benefits of torpor between the sexes by
modeling the energy expenditure of males and females at a single
Ta using several different torpor bout lengths for each
sex and comparing these estimates to normothermic energy expenditure at the
same Ta (Fig.
5). This model estimates energy use during a torpor bout by
summing the torpor maintenance costs (MR duration) and the energetic cost of
arousal. We calculated arousal costs using the following equation (A.
McKechnie, personal communication):
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|
The model suggested that the higher mass-specific metabolic rates of males
lead to slightly greater energy saving for this sex during shorter bouts of
torpor (1-4 h). However, it is evident that females potentially save
substantial energy by using torpor as well. The propensity of females to avoid
torpor during spring suggests that the short-term costs of defending a
normothermic body temperature may be repaid later, perhaps through shorter
embryonic developmental periods and earlier juvenile independence. Our model
calculations are intended for comparison between sexes and probably
overestimate the actual energy expenditure, as they do not account for passive
rewarming from torpor (Geiser and Drury,
2003). Selection of roosts that facilitate passive rewarming may
be an important strategy for reducing energetic costs in bats
(Chruszcz and Barclay, 2002
;
Vaughan and O'Shea, 1976
,
Willis, 2003
). Regardless of
the actual amount of energy saved during torpor under natural conditions, both
sexes potentially benefit to the same degree.
Our data also show how environmental temperature potentially affects torpor
Tb values and energetic savings. Torpid bats maintained
the lowest Tb values at moderate environmental
temperatures (10-15°C), which resulted in the greatest energetic savings.
At Ta<10°C, Tb and MR were more
variable and tended to be higher, resulting in smaller energy savings. Similar
patterns of increasing metabolic rate and body temperature at increasingly low
temperatures by bats in torpor have been observed among lasiurines
(Genoud, 1993) and other
insectivorous species (Hosken and Withers,
1997
). It is unclear whether such variation in response at low air
temperatures is associated with the ability of L. cinereus to
efficiently thermoregulate at temperatures below 10°C or simply an
artefact of our laboratory protocol. We did not choose to run individuals at
low temperatures for >5 h, and the possibility exists that
Tb and MR would have stabilized if we continued
measurements for longer periods. In addition, bats may not reach steady state
minima for extended periods (5-20 h) after torpor is induced
(Riedesel and Williams, 1976
),
thus our measurements may overestimate minimum values. However, Genoud
(1993
) ran L.
cinereus at chamber temperatures <10°C for relatively long time
periods (up to10 h) and observed similar patterns. Our data support Genoud's
argument (Genoud, 1993
) that
sustained periods of torpor (i.e. hibernation) in L. cinereus at
temperatures at or below 0°C are unlikely.
Thermal conductance
At Ta<Tlc, the conductance of
normothermic L. cinereus was 78±2.4% of values expected for
bats, based on body mass alone (Bradley and
Deavers, 1980). Shump and Shump
(1980
) showed that the fur of
L. cinereus provided relatively more insulation than the pelage of
cave-roosting species and attributed the difference to an adaptation for
roosting in foliage versus less exposed sites. Relatively low
conductance values have also been observed in other insectivorous
tree-roosting species (Hosken and Withers,
1997
), but the ubiquity of this pattern in bats that roost in
exposed sites is unclear.
Torpid L. cinereus exhibited lower conductance values than
normothermic individuals. Lower conductance during torpor has also been
observed in rodents (Snyder and Nestler,
1990) and other insectivorous bat species
(Genoud, 1993
;
Hosken, 1997
; Hosken and
Withers, 1997
,
1999
;
Morris et al., 1994
).
Conductance values for male L. cinereus during torpor were
38±5.4% of expected values based on body mass, whereas for the two
females that used torpor values were 3% and 8% of those expected. It is
unclear why conductance is sometimes lower during torpor
(Snyder and Nestler, 1990
),
but possible explanations include changes in breathing rate, posture or
circulation (Hosken and Withers,
1997
).
Sex differences in evaporative water loss rate
Normothermic male L. cinereus exhibited higher mass-specific rates
of EWL than females. In addition, the rate at which males lost water increased
more rapidly as a function of Ta than for females. There
are several potential explanations for higher rates of water loss in males,
including sex differences in breathing rate, body size and metabolism. Among
similarly sized mammals, bats exhibit high rates of transepidermal and
respiratory water loss because of their relatively large wing membranes and
lungs (Bassett, 1980;
Hattingh, 1972
;
Licht and Leitner, 1967
;
Studier, 1970
). Among these
routes of water loss, respiratory losses are probably the highest
(Kurta, 1985
). We measured the
respiratory rates of 32 normothermic individuals and could detect no
significant differences in ventilation frequency between males and females
(t=-0.1, d.f.=30, P=0.94). Differences in
metabolism could also potentially contribute to differences in water loss,
with EWL increasing proportionally with metabolic rate
(Studier, 1970
). Although we
detected metabolic differences between sexes within the thermal neutral zone,
there were no significant differences in rates of mass-specific MR below the
TNZ. However, differences in rates of water loss spanned all measured air
temperatures. These consistent sex differences in EWL, but not MR, suggest
that differences in metabolic rate are not the primary factor influencing sex
differences in evaporative water loss rates. Smaller body size in male L.
cinereus results in higher surface area to volume ratio and
proportionally greater pulmonary and epidermal surface areas of males might
explain the consistently higher rates of water loss over all air temperatures.
Comparable to the findings of the current study, lower rates of water loss in
pregnant females have been observed in other species as well
(Proctor and Studier, 1970
;
Studier, 1970
).
At air temperatures below 25°C, the use of torpor decreased water loss
by as much as 29% in male L. cinereus. Similar reductions in water
loss with torpor use have been noted in other species of temperate
insectivorous bats (Carpenter,
1969; Dwyer, 1971
;
Hosken, 1997
;
Hosken and Withers, 1999
;
Maloney et al., 1999
;
Morris et al., 1994
;
Studier, 1970
). Female L.
cinereus migrate to areas of eastern North America
(Cryan, 2003
;
Findley and Jones, 1964
) where
relative humidity (RH) generally exceeds 50% during summer
(Baldwin, 1968
). Unlike
females, most males remain in arid (<50% RH) regions of western North
America, where evaporative water loss may be problematic. For example, at
rates of water loss measured during this study (1.6-12 mg g-1
h-1), males could potentially lose up to 6-18% of their mass in
body water over the course of a typical 12 h roosting period under hot and dry
conditions. Shump and Shump
(1982
) noted that L.
cinereus could lose up to 28% of its body mass in water without
noticeable effects, but other species suffer high (>50%) mortality after
losing 23-32% of their body mass in water
(Studier et al., 1970
). Given
the vulnerability of foliage-roosting bats to desiccation, torpor may provide
male L. cinereus with a means of saving water in arid regions of
western North America. Although the maintenance of a positive energy budget is
often cited as the principal factor governing summer torpor use in bats, water
balance may also play an important role.
Sex differences in distribution
Selection of optimal microclimates by bats can minimize their
thermoregulatory demands and, in many cases, behavioral thermoregulation may
be just as important as physiological regulation
(Studier and O'Farrell, 1972).
Considering the potential selective advantages for bats that choose roosts
which limit energy and water expenditure, accessibility to sites with adequate
thermal and hygric properties probably plays an important role in determining
species distribution (Baudinette et al.,
2000
; Bell et al.,
1986
; Humphrey,
1975
; Morris et al.,
1994
; Webb et al.,
1995
). However, differences in distribution between sexes of
vespertilionid bats are known to occur at both regional and continental scales
during summer and many of these differences likely stem from differential
energy needs (Barclay, 1991
;
Cryan, 2003
;
Cryan et al., 2000
;
Thomas, 1988
). Are the
different thermoregulatory strategies of male and female L. cinereus
a reflection of their disparate distributions during the summer months? Why do
females forgo so many western areas along their migration route, essentially
flying hundreds of kilometers farther than males? The results of this study
suggest that female L. cinereus may pass through the arid western
regions of North America because climatic conditions there are unfavorable for
raising young. The cooler night-time temperatures and more arid conditions of
western regions during summer (Climate Source, Corvalis, Oregon) would be a
liability to females that remain normothermic. In contrast, males are not
faced with the same energy and water challenges as reproductive females, so
torpor use may mitigate the occupancy of more challenging thermal and hygric
environments found in western North America.
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Acknowledgments |
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