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First published online November 30, 2007
Journal of Experimental Biology 210, 4345-4350 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007294
Energy availability influences microclimate selection of hibernating bats
1 Center for North American Bat Research and Conservation, Department of
Ecology and Organismal Biology, Indiana State University, Terre Haute, IN
47809, USA
2 Department of Biology, University of Regina, Saskatchewan, S4S 0A2,
Canada
3 Department of Ecology and Organismal Biology, Indiana State University,
Terre Haute, IN 47809, USA
* Author for correspondence (e-mail: jboyles3{at}mymail.indstate.edu)
Accepted 30 September 2007
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Key words: Eptesicus fuscus, fat storing, hibernation, metabolic depression, Myotis lucifugus, respirometry, thermal preference
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). Consequently,
hibernating mammals survive winter on a fraction of the energy required to
remain euthermic.
During hibernation, torpid metabolic rate (TMR) is largely
dependent on temperature (Geiser,
1988; Geiser,
2004). Torpid metabolic rate drops exponentially to a minimum
temperature (Tmin) and then increases rapidly as ambient
temperature (Ta) falls below Tmin. The
Ta at which TMR is minimal varies by species and
is often considered the optimal temperature for energy conservation during
hibernation. In addition, the length of torpor bouts increases as
Ta decreases, thereby minimizing the frequency of
energetically expensive arousal bouts
(Brack and Twente, 1985;
Dunbar and Tomasi, 2006).
Individuals may maximize winter survival and optimize their energetic
condition for spring emergence by choosing a hibernaculum with
Ta near Tmin
(Richter et al., 1993;
Tuttle and Kennedy, 2002).
Migration and gestation in spring often start shortly after hibernation
(Kunz et al., 1998;
Michener, 1985), so emerging
from hibernation with a larger energy reserve may confer a reproductive
advantage over individuals with small energy reserves
(Hackländer and Arnold,
1999; King et al.,
1991).
However, factors other than energetic constraints may also influence
hibernation decisions. For instance, it has been proposed that hibernation
imposes ecological costs such as decreased detection of predators
(Humphries et al., 2003a) and
increased likelihood of freezing (Clawson
et al., 1980). Hibernation may also have physiological costs such
as reduced motor function (Choi et al.,
1998), decreased immune response
(Luis and Hudson, 2006;
Prendergast et al., 2002),
sleep deprivation (Daan et al.,
1991; Trachsel et al.,
1991) and reduced protein synthesis
(Frerichs et al., 1998;
Van Breukelen and Martin,
2002). An optimization approach predicts that hibernating mammals
should minimize these negative aspects of hibernation while maintaining
sufficient energy reserves to survive winter (referred to herein as the
`hibernation optimization hypothesis')
(Humphries et al., 2003a). As
such, individuals with high energy availability should exhibit less frequent,
shorter and shallower (i.e. maintenance of a higher Tb)
torpor bouts compared with individuals with smaller energy reserves. As
predicted by the hibernation optimization hypothesis, food-caching eastern
chipmunks, Tamias striatus, express shorter and shallower hibernation
bouts when food hoards are supplemented
(French, 2000;
Humphries et al., 2003b). This
suggests that the physiological and ecological costs of hibernation are
substantial and may be avoided when energetically feasible.
Recent evidence suggests that fat-storing hibernators also minimize the
expression of hibernation when stored energy (body fat) is abundant. By
spending less time in torpor and maintaining a higher Tb
during torpor, individuals with sufficient energy stores may minimize the
costs of hibernation (Wojciechowski et
al., 2007). Fat-storing species generally cannot increase energy
intake as can food-caching species (e.g.
Humphries et al., 2003b);
however, they can behaviorally regulate the length and depth of torpor by
selecting favorable microclimates (Brack
and Twente, 1985; Kokurewicz,
2004). Hibernating at warm temperatures leads to increased energy
expenditure (Dunbar and Tomasi,
2006; Geiser,
2004) but a high Tb also minimizes the
expression of torpor and should therefore lessen negative aspects of
hibernation (Humphries et al.,
2003a). Individuals with large fat stores should be more
energetically capable of hibernating at warmer temperatures than individuals
with small fat stores and may therefore choose warmer temperatures to lessen
the ecological and physiological costs of hibernation
(Munro et al., 2005).
We tested the hypothesis that energy availability affects microclimate selection of fat-storing hibernators using two species of vespertilionid bats, the little brown myotis, Myotis lucifugus (LeConte 1831), and the big brown bat, Eptesicus fuscus (Beauvois 1796). In a correlative field study, we predicted that hibernating individuals would select hibernation temperatures according to their body mass: energetically constrained individuals (i.e. individuals with less body fat) should minimize energy expenditure by hibernating at cooler temperatures, while less energetically constrained individuals should minimize the costs of hibernation by selecting warmer temperatures. In a laboratory study, we sought to determine if experimental manipulation of energy availability [via the drug mercaptoacetate (MA)] influenced microclimate selection during hibernation. We predicted that experimental limitation of energy availability would cause bats to choose cooler microclimates than control individuals.
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Materials and methods |
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). Therefore,
little brown myotis were used to examine microclimate selection in a natural
setting. Big brown bats hibernate in buildings, mines, caves and trees and are
known for their hardiness, ease of care in captivity
(Wilson, 1988) and ability to
hibernate and become active across a wide range of temperatures
(Boyles et al., 2006). They are
an ideal model for testing microclimate selection in the laboratory through
experimental energy manipulations.
Field experiment
We studied a population of hibernating little brown myotis in an abandoned
limestone mine in western Ohio, USA, during the winter of 2006–2007. The
mine contains approximately 71 km of passages and is surveyed biennially for
endangered Indiana myotis, Myotis sodalis. During these surveys, rock
temperature is mapped throughout the mine, and little brown myotis typically
hibernate across approximately a 12°C (0–12°C) thermal gradient
(Brack, 2007). The winter of
2006–2007 was an El Niño year, and thus weather patterns were
atypical. The regional temperature was approximately 4°C above the
long-term monthly mean in December and January and 7°C below the mean in
February (National Oceanic and Atmospheric Administration, Dayton, OH Weather
Station). Because of the delayed onset of cold temperatures, the rock
temperatures across which little brown myotis were hibernating was only
3°C and bats were not as abundant as in previous years
(Brack, 2007).
We collected data on three dates during the hibernation season: 2 December
2006, 14 January 2007 and 12 February 2007. For each bat or cluster, we
measured rock temperature within 3 cm of the cluster and air temperature
within 7 cm of the cluster using a thermocouple thermometer (Model 52 II;
Fluke Corporation, Everett, WA, USA) accurate to 0.1°C. The thermometer
was factory-calibrated and the calibration was verified in an ice bath in the
field before measurements were taken. We weighed bats using a digital balance
accurate to 0.1 g (Scout II; Ohaus, Pine Brook, NJ, USA) and measured forearm
length to the nearest mm to adjust mass for body size. Mass alone (or mass
corrected for forearm length) is not necessarily indicative of fat mass.
However, body mass and fat mass are highly correlated in little brown myotis
(Kunz et al., 1998). Following
data collection, we released bats on a surface near where they were
collected.
We split the collection area into two halves (front and back), designated
by an obvious physical break in the mine
(Brack, 2007). We predicted
that bats hibernating in the warmer, back half of the mine would be larger
than bats hibernating in the cooler, front half of the mine; therefore, we
tested for differences in body mass of individuals in the two areas using
one-tailed t-tests (Zar,
1999).
Laboratory experiments
We collected 20 adult big brown bats (10 male, 10 female) from December
2006 to February 2007 in the attic of an unused school building in western
Indiana and from an abandoned limestone mine in western Ohio. We transferred
bats to holding facilities at Indiana State University where they were kept
communally in soft mesh cages (43x43x38 cm) at 8.5±1°C.
Bats were not fed before trials to ensure they were post-absorptive but were
fed mealworm, Tenebrio molitor, larvae prior to release, and water
was available ad libitum.
Thermal preference
Stored body fat is the main source of energy for bats during hibernation
(Dark, 2005). Therefore, we
assessed the thermal preference of hibernating big brown bats before and after
manipulating their energetic state with mercaptoacetate (Sigma, St Louis, MO,
USA). MA inhibits fatty acid availability by reducing the mitochondrial
oxidation of fatty acids (Bauche et al.,
1983; Dark and Miller,
1998). MA increases food intake in rats on high-fat diets
(Scharrer and Langhans, 1986)
and affects torpor expression in placental golden-mantled ground squirrels,
Spermophilus lateralis (Dark and
Miller, 1998), and marsupial eastern pygmy possums,
Cercartetus nanus (Westman and
Geiser, 2004). In eastern pygmy possums, Tb
and TMR of individuals injected with MA did not differ significantly
from food-deprived individuals (Westman
and Geiser, 2004). Dosages of MA used herein are sufficient to
cause a substantial increase in food intake in rats
(Scharrer and Langhans, 1986),
indicating an inhibition of fatty acid oxidation. However, they are low enough
that ground squirrels were not aroused from hibernation
(Dark and Miller, 1998), which
is important because our experiment requires bats to enter torpor.
To test the thermal preference of hibernating bats, we established a thermal gradient on a 127x61x0.3 cm sheet of aluminum placed in a dark, walk-in environmental chamber set at 6.0±1°C. The apparatus was laid flat on a shelf and covered with soft mesh so bats could move along the gradient. We placed a strip of terrarium heat tape (Flexwatt, Calorique Ltd, West Wareham, MA, USA) running at full power on one end of the aluminum sheet and a second strip of terrarium heat tape running at half power near the midpoint of the aluminum. We covered the underside of the aluminum sheet, including the heat tape, with insulation. This created a thermal gradient running from approximately 6.0°C on one end of the aluminum sheet to 12.5°C on the opposite end. We covered the apparatus with a large plastic container to keep bats on the gradient. We hung black cloth inside the container such that it lightly touched the gradient (Fig. 1). This homogenized the structure within the apparatus, allowing hibernation location to be selected based on temperature; without the cloth, bats hibernated exclusively touching one edge of the lid.
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). Treatment for each individual was determined by a random
number generator. After injection, we held bats at room temperature
(22±1°C) for 15–20 min before placing them onto the thermal
gradient. We left bats on the gradient for 6–18 h, removed them and
recorded the temperature where they hibernated as described above. Trials were
conducted in January and February 2007.
Treatment with MA should mimic energy limitation. According to the
hibernation optimization hypothesis, energy-limited bats should choose colder
temperatures for hibernation to maximize energy savings, while energetically
capable individuals should choose warmer temperatures to minimize the negative
aspects of hibernation. We predicted that bats treated with MA would exhibit a
significantly larger decrease in temperature of hibernation than bats given
the control. Therefore, we used one-tailed t-tests to determine if
the difference in temperature selected before and after the injection was
larger in the MA group than in the control group
(Zar, 1999).
Respirometry
Mercaptoacetate lowers TMR and Tb in some
eastern pygmy possums, a hibernating marsupial
(Westman and Geiser, 2004). In
placental mammals, Tb is not lowered
(Dark and Miller, 1998) or is
lowered only slightly (Stamper and Dark,
1997), and the effect of MA on TMR is unknown. A drop in
TMR caused by MA should lessen the strength of the effect in the
thermal preference experiment because a smaller change in hibernating
temperature would be needed to lower TMR to the necessary level.
To determine whether handling stress and injection of MA influenced
TMR, we measured oxygen consumption of torpid adult female big brown
bats not used in the thermal preference experiment, using open-airflow
respirometry before and after injection of MA (400 µmol
kg–1). We placed individual bats in a metabolic chamber
consisting of a sealed 0.24-liter glass jar lined with nylon netting so bats
could hang freely. The metabolic chambers were placed in a
temperature-controlled chamber maintained at 10°C. Temperature was not
measured in the metabolic chambers, so the bat's body heat could have slightly
raised Ta. Ambient air was dried and pushed through the
metabolic chamber at 100 ml min–1. Incurrent air flow was
measured with a factory-calibrated mass flow controller (Sable Systems, Las
Vegas, NV, USA). Excurrent air was scrubbed of carbon dioxide and water with
soda lime and anhydrous calcium sulfate, respectively, before passing into an
oxygen analyzer (FC-10A; Sable Systems). We calibrated the oxygen analyzer to
ambient air prior to respirometry trials. We kept the bats in the metabolic
chamber for approximately 4 h before each trial to allow oxygen consumption to
stabilize before measurements were recorded. We ran trials for 2 h and began
all trials during the inactive part of the bats' daily cycle. Fractional
oxygen concentrations were recorded at 1 min intervals, and we identified the
minimum value (from 10 min means) for each individual before and after
administration of MA. We calculated oxygen consumption corrected for standard
temperature and pressure
(
O2) using the
methods of Withers (Withers,
2001). Data were analyzed for whole-animal (ml O2
h–1) and mass-specific values (ml O2
h–1 g–1). We used 0.179 ml O2
h–1=1 mW for conversion from
O2 to
TMR (Willis et al.,
2005).
Respirometry measurements were limited because of the availability of bats and time constraints on equipment. All trials were performed at 10°C, near the temperature in the center of the thermal gradient, because our goal was only to determine if handling effects or injection of MA caused a drop in TMR, not to quantify a change in TMR across a range of temperatures. Further, we did not use a control group in respirometry experiments to differentiate between handling effects and treatment effects, because this is inconsequential to the results of our study. We used respirometry results only to strengthen our conclusion in the thermal preference experiment.
We calculated statistics in Minitab version 14 (State College, PA, USA). Results are reported as means (± s.d.). All field and laboratory methods were approved by the Indiana State University Animal Care and Use Committee under protocol JOW/JB 9-18-2006.
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0.25–0.47 for all comparisons) but
were detectable and were always in the predicted direction (i.e. larger bats
were at warmer temperatures). We would not expect all six comparisons to be
significant in the same direction if this significance is purely artifactual.
These differences, if assumed to be solely related to differences in fat mass,
represent 
10% of fat mass acquired prior to the onset of hibernation in
little brown myotis (Kunz et al.,
1998).
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Respirometry
Injection of MA caused a drop in whole-animal
O2 at 10°C
from 0.39±0.29 ml O2 h–1 to
0.22±0.15 ml O2 h–1 and a drop in
mass-specific O2
from 0.022±0.015 ml O2 h–1
g–1 to 0.019±0.008 ml O2
h–1 g–1. This equates to a marginally
significant drop in whole-animal TMR from 2.18±1.63 mW to
1.25±0.88 mW (paired t-test, d.f.=8, t=2.22,
P=0.057) and a drop in mass-specific TMR from
0.124±0.084 mW g–1 to 0.072±0.045 mW
g–1 (paired t-test, d.f.=8, t=2.15,
P=0.069). This change represents a 43% decrease in whole-animal
TMR and a 42% decrease in mass-specific TMR after injection
of MA. Although the drop is non-significant, the effect size of MA is very
large on both whole-animal TMR (Hedges' =2.04) and
mass-specific TMR (Hedges' =1.87).
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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;
Humphries et al., 2003b) using
fat-storing hibernators. Our results suggest that energy availability affects
microclimate selection during hibernation in these two fat-storing bat
species. As predicted by the hibernation optimization hypothesis, body mass
was related to microclimate selection in little brown myotis. Field data
indicate that heavier, and presumably fatter (sensu
Kunz et al., 1998),
individuals selected warmer temperatures for hibernation than did smaller
individuals. Natural variation in hibernation microclimate matched the
predicted pattern in both sexes on all three sampling occasions, despite the
unusually warm winter and narrow thermal gradient in the mine. We expect the
difference in microclimate selection to be more pronounced during a normal
winter when a larger thermal gradient is present. Furthermore, this pattern
was apparent despite evidence that individuals in clusters are heavier than
solitary individuals (Fenton,
1970) and nearly all clusters in our experiment were in the front,
colder section of the mine. Likewise, experimental reduction of fat availability with MA caused individuals to choose colder temperatures for hibernation. This pattern emerged despite a nearly significant drop in TMR due to handling and the injection of MA. The nearly significant P-value and large effect size give us cause to believe this relationship is biologically important. It suggests that physiological mechanisms did not decrease TMR sufficiently and bats used microclimate selection to slow TMR even further. Our results suggest that energetic state influences the thermal preference of hibernation sites in fat-storing hibernators such as big brown bats.
Unlike food-caching species, fat-storing hibernators generally cannot
adjust energy intake during hibernation; therefore, survival costs are
potentially large if an animal expends energy too quickly or if an unusually
harsh winter extends the hibernation season
(Dark, 2005). Regardless, our
results, and those of Wojciechowski et al.
(Wojciechowski et al., 2007),
indicate that fat-storing bats minimize their expression of torpor when energy
reserves are sufficient. Our results suggest that fat-storing bats regulate
the expression of torpor through microclimate selection, while Wojciechowski
et al. (Wojciechowski et al.,
2007) suggest torpor is regulated by changes in depth and length
of torpor bouts. These differences may be explained by interspecific
variation, but it is likely that both microclimate selection and changes in
depth and length of torpor bouts are important mechanisms of hibernation
regulation.
Our results add to the growing literature suggesting that the optimal
hibernation strategy may not be characterized by long, deep bouts of torpor to
minimize energy expenditure (Humphries et
al., 2003b). Rather, the optimal hibernation strategy for
fat-storing bats (and likely other fat-storing species) may be to hibernate at
a relatively warm Ta (which will lead to a high
Tb and short torpor bouts), thereby minimizing the
ecological and physiological costs of hibernation. The optimal expression of
torpor is likely to be different for each individual. This may explain
intraspecific variation in temperature selection by hibernating bats, and thus
the locations and temperatures at which individuals are found hibernating in
caves and mines. To our knowledge, this is the first mechanistic hypothesis
explaining intraspecific variation in microhabitat selection by fat-storing
species during hibernation. It may also provide clues for understanding
interspecific variation in microclimate selection
(McNab, 1974), although this
is speculative without further experiments. Other factors, such as the
decreased probability of predation in the back of a hibernacula
(Kokurewicz, 2004), may help
explain why not all individuals hibernate at the temperature that minimizes
energy expenditure. However, the ability to take advantage of any such
benefits is ultimately constrained by energetic considerations.
This study has important conservation and management implications for bats
during the hibernation season. It has been suggested that ideal hibernacula
are cold and thermally stable (sensu
Tuttle and Kennedy, 2002).
Hibernacula meeting these criteria may minimize energy expenditure but they
also limit the opportunity for individuals with sufficient energetic reserves
to choose warmer microclimates and minimize negative aspects of hibernation.
In addition, the energetic savings from hibernating at cold temperatures may
be outweighed by unknown long-term fitness costs (e.g. lowered survival or
reproduction) of hibernating at those temperatures.
In summary, our results suggest that energy availability affects microclimate selection of hibernating bat species. Minimizing energy expenditure may be the ultimate goal of hibernation, but hibernation is not a cost-free strategy and may be avoided when possible. Presumably, there must be a benefit to hibernating at warmer temperatures to offset the added energetic costs; otherwise, all individuals would hibernate at the temperature that minimizes energy expenditure. Further research is needed to determine what these benefits are and the ecological (e.g. risk of freezing or predation) and physiological (e.g. buildup of metabolic waste) costs that cause hibernators to avoid cold temperatures when energetically capable.
List of abbreviations
O2
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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