Am J Physiol Regulatory Integrative Comp Physiol
279: R255–R262, 2000.
Effects of ambient temperature on metabolic rate,
respiratory quotient, and torpor in an arctic hibernator
C. LOREN BUCK AND BRIAN M. BARNES
Institute of Arctic Biology and Department of Biology and Wildlife,
University of Alaska Fairbanks, Fairbanks, Alaska 99775
Received 27 July 1999; accepted in final form 2 February 2000
hibernation; metabolism; arctic ground squirrel; metabolic
fuel
their energy requirements
during a prolonged dormant season by becoming hypometabolic and hypothermic (5, 60). Several physiological mechanisms have been proposed for the reduced
metabolism that leads to energy savings during hibernation. These include temperature-dependent or Q10
effects on enzyme kinetics (22, 48), temperature-independent or active suppression of metabolism (53), combined temperature-dependent and -independent inhibition (25, 50, 51), temperature differential effects (28),
and low thermal conductance during torpor (49). Distinguishing among these mechanisms requires deHIBERNATING MAMMALS REDUCE
Address for reprint requests and other correspondence: B. M.
Barnes, Institute of Arctic Biology, Univ. of Alaska Fairbanks, Fairbanks, Alaska 99775 (E-mail: ffbmb@uaf.edu).
http://www.ajpregu.org
tailed measurements of body temperature and metabolism over a wide range of ambient temperatures,
including levels below which hibernators begin to regulate their body temperature (51), and investigations
at biochemical and molecular levels to identify unique
or differential gene regulation related to energy metabolism across the stages of hibernation (6).
The hypometabolic and hypothermic state in hibernators cannot be sustained for more than several
weeks, and instead, torpor is regularly interrupted by
arousals to euthermia (58). The functional significance
of these arousal episodes is not known, but hypotheses
generally relate to either metabolic rate and metabolic
fuel-dependent processes or, alternatively, body temperature-dependent processes. Separating effects of
metabolic rate and body temperature on frequency of
arousals and thus torpor bout length requires investigations over a wide range of ambient temperature (Ta)
over which metabolic rate and body temperature become uncoupled.
Although ample comparative data have been published on metabolic rate during torpor (TMR) and metabolic fuel use of mammalian hibernation during torpor at Ta values ⬎0°C, only a few studies have been
done at Ta slightly below 0°C (1, 25, 29) and none in the
conditions that prevail in hibernacula in the arctic (⫺5
to ⫺25°C) (2, 9). To determine the energetic costs and
substrate use associated with hibernation under arctic
conditions, we measured core body temperature (Tb),
TMR, and respiratory quotient (RQ) of arctic ground
squirrels (Spermophilus parryii) in steady-state torpor
at subzero Ta values from 0 to ⫺16°C. To further
investigate relationships between TMR, conductance,
and Ta and to investigate temperature-independent
inhibition of metabolic rate in hibernating arctic
ground squirrels, we extended measurements to Ta
values of 0–20°C. To examine how torpor bout length
changes in response to changes in Tb, Ta, TMR, and
metabolic fuel use, in parallel experiments we measured frequency of arousal episodes in a group of undisturbed arctic ground squirrels at Ta values ranging
from ⫺16 to 20°C.
The costs of publication of this article were defrayed in part by the
payment of page charges. The article must therefore be hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. Section 1734
solely to indicate this fact.
0363-6119/00 $5.00 Copyright © 2000 the American Physiological Society
R255
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
Buck, C. Loren, and Brian M. Barnes. Effects of ambient temperature on metabolic rate, respiratory quotient, and
torpor in an arctic hibernator. Am J Physiol Regulatory
Integrative Comp Physiol 279: R255–R262, 2000.—Arctic
ground squirrels (Spermophilus parryii) overwinter in hibernaculum conditions that are substantially below freezing.
During torpor, captive arctic ground squirrels displayed ambient temperature (Ta)-dependent patterns of core body temperature (Tb), metabolic rate (TMR), and metabolic fuel use,
as determined by respiratory quotient (RQ). At Ta 0 to
⫺16°C, Tb remained relatively constant, and TMR rose proportionally with the expanding gradient between Tb and Ta,
increasing ⬎15-fold from a minimum of 0.0115 ⫾ 0.0012 ml
O2 䡠 g⫺1 䡠 h⫺1. At Ta 0–20°C, Tb increased with Ta; however,
TMR did not change significantly from Tb 0 to 12°C, indicating temperature-independent inhibition of metabolic rate.
The overall change in TMR from Tb 4 to 20° equates to a Q10
of 2.4, but within this range of Tb, Q10 changed from 1.0 to
14.1. During steady-state torpor at Ta 4 and 8°C, RQ averaged 0.70 ⫾ 0.013, indicating exclusive lipid catabolism. At
Ta ⫺16 and 20°C, RQ increased significantly to ⬎0.85, consistent with recruitment of nonlipid fuels. RQ was negatively
correlated with maximum torpor bout length. For Ta values
⬍0°C, this relationship supports the hypothesis that availability of nonlipid metabolic fuels limits torpor duration in
hibernating mammals; for Ta values ⬎0°C, hypotheses
linked to body temperature are supported. Because anterior
body temperatures differ from core, overall, the duration
torpor can be extended in hibernating mammals may be
dependent on brain temperature.
R256
METABOLISM AND TORPOR
METHODS
RESULTS
Thermoregulatory patterns during torpor at differing
Ta. Patterns of thermoregulatory heat production of
arctic ground squirrels hibernating at different Ta values depended on whether Ta was higher or lower than
0°C. At Ta values ⬍0°C, all animals increased rates of
thermogenesis to maintain a relatively constant Tb. At
Ta values ⬎0°C, animals maintained minimal levels of
heat production as Tb varied with Ta (Fig. 1). At Ta 0°C,
three of eight animals had increased rates of thermoregulatory heat production as indicated by a greater
⌬T (Tb ⫺ Ta), which ranged from 1.20 to 1.26°C, and an
elevated TMR, averaging 0.020 ⫾ 0.0027. These values
were significantly greater than corresponding values
in the remaining five animals of ⌬T averaging 0.52°C
(P ⬍ 0.05) and TMR averaging 0.014 ⫾ 0.0004
(P ⬍ 0.05). From these results, we considered torpid
animals to be actively thermoregulating if ⌬T was
⬎1°C.
At Ta values ⬍0°C, Tb averaged ⫺0.42 ⫾ 0.12°C and
did not change significantly with changing Ta (P ⫽
0.071, N ⫽ 8, n ⫽ 24; Fig. 1). The lowest Tb recorded
was ⫺1.97°C at Ta ⫺8°C. From its minimum value of
0.0115 ⫾ 0.0012 ml O2 䡠 g⫺1 䡠 h⫺1 at Ta 4°C, TMR
increased 15.8-fold to 0.182 ⫾ 0.0244 ml O2 䡠 g⫺1 䡠 h⫺1
at ⫺16°C (Fig. 1). Between Ta ⫺4 and ⫺16°C, TMR was
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
Animals. Arctic ground squirrels (S. p. kennicottii) were
live-trapped in July in the northern foothills of the Brooks
Range, Alaska, near the Atigun River (68° 38’ N latitude) and
transported to the animal holding facility at the University of
Alaska Fairbanks. Animals were maintained individually in
metal cages (45.7 ⫻ 30.5 ⫻ 20.3 cm) at a photoperiod of
12:12-h light-dark cycle and Ta of 5 ⫾ 2°C before the beginning of the experiment. Food (Mazuri Rodent Chow, carrots,
and sunflower seeds) and water were provided ad libitum.
Body temperature. To record Tb, temperature-sensitive radiotransmitters (model VMH-BB, Minimitter, Sunriver, OR)
were surgically implanted into each animal’s peritoneal cavity at least 1 mo before the start of metabolic measurements.
For surgery, animals were anesthetized with methoxyflurane. Beforehand, transmitters were calibrated to the nearest 0.1°C against a precision mercury thermometer in a
waterbath at 0 and 20°C. Animals were held at Ta 20°C after
surgery for 7 days and then transferred to 15-liter plastic
respirometry chambers housed in a temperature-controlled
environmental chamber. Cotton batting was provided for
nesting material, and cages were filled to 5 cm with absorbent wood chips. The signal from the transmitter was received with a model RA1010 radio receiver that was interfaced to a computerized system of data acquisition
(Dataquest III, Minimitter) and recorded once per 15-min
interval. The University of Alaska Fairbanks’ institutional
animal care and use committee approved all procedures.
Respirometry. Rates of oxygen consumption and carbon
dioxide production were recorded during steady-state torpor
for eight adult animals (4 male, 4 female) at Ta ⫺16, ⫺8, ⫺4,
0, 4, 8, 12, 16, and 20°C (each ⫾0.5°C). Metabolic measures
were not recorded from all eight animals at Ta 8–20°C because not all animals continued to hibernate at these relatively high temperatures. Animals were tested after they had
been in hibernation for at least 1 mo, and measurements of
TMR began 4 days after Tb of each subject animal had
decreased to below 30°C during entry into a torpor bout. TMR
was measured of animals within their nests at Ta values ⫺16
to 20°C and, in addition, at Ta values of ⫺8, ⫺4, 0, and 4°C
from animals that were removed from their nests and placed
on wood chips. Rates of oxygen consumption and carbon
dioxide production were recorded each 1 min over 5 h of
torpor for each animal at each Ta. A flow rate of 125–300
ml/min (depending on mass and TMR of the animal) of dried
air was delivered through the respirometry chamber with a
flow rotometer and measured with a mass flowmeter (model
229H, Teldyne Hastings-Raydist, Hampton, VA). Dried air
leaving the respirometry chamber was measured for oxygen
content with a single-channel oxygen analyzer (Ametek Applied Electrochemistry S-3A, Pittsburgh, PA) and for carbon
dioxide content with a carbon dioxide analyzer (Beckman
model 864 infrared CO2 analyzer, Fullerton, CA). Rates of
oxygen consumption and carbon dioxide production were
defined for each Ta as the mean rate measured over the last
1 h of (60 measures) of steady-state torpor, i.e., constant Tb
and rate of oxygen consumption for 2 or more consecutive
hours. Carbon dioxide and oxygen analyzers were calibrated
to outside air and span gas (20% O2 and 0.5% CO2) at 1-h
intervals during the metabolic trial. Equation 3b of Withers
(64) was used to calculate rates of oxygen consumption. The
mass specific apparent conductance (C) was calculated as
C ⫽ TMR/(Tb ⫺ Ta) and Q10 of metabolic rate as Q10 ⫽
(TMR1/TMR2)(10/Tb1 ⫺ Tb2). To estimate rates of carbohydrate
use by hibernating arctic ground squirrels, which apparently
do not catabolize lean tissue during torpor (20), we converted
the product of the RQ and TMR to protein free rates of
carbohydrate utilization by relating RQ to proportions of
carbohydrate consumed (32). This proportion was multiplied
by the TMR and converted using 0.84 l O2/g carbohydrate
equivalent.
In a parallel experiment using a separate group of wild
caught adult arctic ground squirrels of mixed sex, the maximum torpor bout length (TBL) of animals left undisturbed
within their nests was determined for Ta ⫺16, ⫺8, ⫺4, 0, 4,
10, 16, and 20°C. Surgeries to implant temperature-sensitive
radiotransmitters were completed at least 1 mo before hibernation using the same protocol as with animals in the metabolism experiment. TBL was calculated as the number of
hours Tb was ⬍30°C as measured by radiotelemetry. The
longest bout of torpor for each individual was recorded as its
TBL for each Ta and averaged with values of TBL of other
animals.
Data are presented as means ⫾ SE. Statistical evaluations
of multiple group comparisons were completed with a oneway ANOVA and pairwise comparisons with a Tukey’s test.
A Student’s t-test was used for between-group comparisons,
and nonnormally distributed data were analyzed with a
Mann-Whitney’s rank sum test (66). A simple linear regression model was used to test for significant correlations between variables. For regression analysis, TMR results for Ta
values ⬎0°C were log transformed to meet the assumptions
of equal variance. We compared the coefficient of determination (r2) to select between linear and curvilinear models. RQ
data were transformed (arcsin square root transformation)
before analysis to meet the assumptions of normality for
parametric tests. In reporting sample sizes, N represents the
number of animals and n the number of measurements.
Because the regression analyses violate assumptions of independence and may underestimate ␣ due to pseudoreplication,
differences were considered significant at P ⬍ 0.01. Differences were considered significant at P ⬍ 0.05 for nonregression analyses.
R257
METABOLISM AND TORPOR
positively and linearly correlated with ⌬T (r2 ⫽ 0.95,
P ⬍ 0.001, N ⫽ 8, n ⫽ 24) but not Tb (r2 ⫽ 0.008, P ⫽
0.685, N ⫽ 8, n ⫽ 24). At Ta values ⬎0, ⌬T averaged
0.61 ⫾ 0.12°C and was not significantly correlated to
TMR (P ⫽ 0.184, N ⫽ 8, n ⫽ 35).
At Ta values ⬎0°C, Tb increased linearly with Ta
(r2 ⫽ 0.99, P ⬍ 0.001, N ⫽ 9, n ⫽ 35; Fig. 1). However,
TMR did not differ significantly between Ta 4 and 12°C
(P ⬎ 0.05, N ⫽ 9, n ⫽ 24), even though over this range
Tb increased on average 7.9°C. TMR at Ta 16°C
(0.0179 ⫾ 0.005 ml O2 䡠 g⫺1 䡠 h⫺1) and Ta 20°C
(0.0466 ⫾ 0.007 ml O2 䡠 g⫺1 䡠 h⫺1) were significantly
higher compared with TMR at Ta 4°C (P ⬍ 0.05). In a
stepwise linear regression including Tb, Ta, and ⌬T, the
increase in TMR from Ta 4 to 20°C was significantly
correlated only to Tb and is best described with an
exponential regression (r2 ⫽ 0.56, P ⬍ 0.001, N ⫽ 9,
n ⫽ 35). The overall increase in steady-state TMR from
Ta 4 to 20°C reflects a Q10 of 2.4; however, Q10 varied
within this range of Ta values from 1 to 14.1 (Table 1).
Conductance of torpid arctic ground squirrels in
nests at Ta values ⱕ0°C averaged 0.012 ⫾ 0.0005 ml
O2 䡠 g⫺1 䡠 h⫺1 䡠 °C⫺1 and was not significantly correlated
to either Ta (r2 ⫽ 0.013, P ⫽ 0.597, N ⫽ 9, n ⫽ 24) or Tb
(r2 ⫽ 0.114, P ⫽ 0.106, N ⫽ 9, n ⫽ 24). At Ta values
⬎0°C, conductance was significantly greater than at Ta
values ⬍0 (P ⫽ 0.001) and averaged 0.043 ⫾ 0.009 ml
O2 䡠 g⫺1 䡠 h⫺1 䡠 °C⫺1. Conductance at Ta values ⬎0°C
was not significantly correlated to either Tb (r2 ⫽ 0.270,
P ⫽ 0.026, N ⫽ 11, n ⫽ 43) or Ta (r2 ⫽ 0.173, P ⫽ 0.012,
N ⫽ 11, n ⫽ 43).
Influence of a nest. We compared Tb and TMR of
eight torpid arctic ground squirrels hibernating with
and without nest material at Ta 4 to ⫺8°C. As indicated
by ⌬T either greater or less than 1°C, three of eight
animals with or without nests had increased thermoregulatory heat production at Ta 0°C (⌬T ⫽ 1.17, 1.24,
and 1.27°C), all had at Ta ⫺4 and ⫺8°C (⌬T ⫽ 3.38–
7.98°C), and none had at 4°C (⌬T ⫽ 0.16–0.80°C).
There was no difference in TMR of animals hibernating
Table 1. Ta, Tb, and average TMR of arctic ground
squirrels during steady-state torpor and
corresponding Q10 values of TMR between
different Tb measurements
Group
Ta, °C
Tb, °C
TMR, ml
O2 䡠 g⫺1 䡠 h⫺1
1
2
3
4
5
4
4.66
8
8.22
12
12.56
16
17.11
20
20.73
0.0115
0.0115
0.0137
0.0179
0.0466
Q10 values
Q10(1⫺2)
Q10(1⫺3)
Q10(1⫺4)
Q10(1⫺5)
⫽
⫽
⫽
⫽
1.0
1.25
1.43
2.4
Q10(2⫺3)
Q10(2⫺4)
Q10(2⫺5)
Q10(3⫺4)
⫽
⫽
⫽
⫽
1.5
1.64
3.06
1.8
Q10(3⫺5) ⫽ 4.45
Q10(4⫺5) ⫽ 14.1
Ta, ambient temperature; Tb, average body temperature; TMR,
maximum torpid metabolic rate.
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
Fig. 1. Effect of ambient temperature (Ta) on metabolic rate measured as rate of oxygen consumption, core body temperature (Tb),
and respiratory quotient of arctic ground squirrels during steadystate torpor. Values are means ⫾ SE; N refers to number of animals
contributing to each mean.
with a nest vs. without a nest at Ta 4°C (P ⫽ 0.559, N ⫽
8, n ⫽ 16) and 0°C (P ⫽ 0.286, N ⫽ 8, n ⫽ 16). At Ta
values ⬍0°C, TMR of animals hibernating without a
nest was significantly higher than within a nest at the
same Ta (32.3% at ⫺4°C and 35.8% at ⫺8°C; P ⬍ 0.05,
N ⫽ 8, n ⫽ 32). This difference can be attributed to
significantly higher conductance for animals without a
nest at both Ta ⫺4°C (mean conductance in a nest ⫽
0.0107 ⫾ 0.001 ml O2 䡠 g⫺1 䡠 h⫺1 䡠 °C⫺1, without a nest ⫽
0.0170 ⫾ 0.001 ml O2 䡠 g⫺1 䡠 h⫺1 䡠 °C⫺1; P ⬍ 0.001, N ⫽
8, n ⫽ 16) and at Ta ⫺8°C (mean conductance in a
nest ⫽ 0.0124 ⫾ 0.0003 ml O2 䡠 g⫺1 䡠 h⫺1 䡠 °C⫺1, without
a nest ⫽ 0.0195 ⫾ 0.0008 ml O2 䡠 g⫺1 䡠 h⫺1 䡠 °C⫺1;
P ⬍ 0.001, N ⫽ 8, n ⫽ 16).
Fuels of metabolism. To identify the metabolic fuels
used during torpor, we calculated the RQ for ground
squirrels hibernating at different Ta. Mean RQ of
0.70 ⫾ 0.013 at Ta 4 and 8°C increased at lower and
higher Ta values, reaching significantly higher values
of 0.86 ⫾ 0.021 at Ta ⫺16°C (P ⬍ 0.05) and 0.88 ⫾ 0.085
at Ta 20°C (P ⬍ 0.05; Fig. 1). At Ta values ⬍0°C, RQ
positively correlated with TMR (r2 ⫽ 0.409, P ⬍ 0.001,
N ⫽ 8, n ⫽ 24) but not Tb (r2 ⫽ 0.017, P ⫽ 0.540, N ⫽
8, n ⫽ 24). At Ta values ⬎0°C, RQ was positively
correlated with Tb (r2 ⫽ 0.523, P ⬍ 0.001, N ⫽ 8, n ⫽
35), and addition of TMR or Ta in a stepwise regression
model did not significantly improve the fit of the regression model.
TBL. Maximum TBL of undisturbed animals was
longest at Ta 0°C, averaging 15.1 days, and did not
change significantly between Ta ⫺4 and 4°C (P ⬎ 0.05;
Fig. 2). Compared with Ta at 0°C, TBL was significantly shorter at Ta values less than or equal to ⫺8°C
and ⱖ10°C. To investigate interrelationships of TBL to
TMR, Tb, and RQ at differing Ta, we performed linear
stepwise regression analyses. Averages of TBL of undisturbed arctic ground squirrels hibernating at Ta
⫺16 to 20°C were regressed with averages of TMR, Tb,
and RQ from animals monitored for respirometry at
the corresponding Ta (with the exception of comparing
R258
METABOLISM AND TORPOR
TBL of animals held at Ta 10°C with respirometry and
Tb values of animals held at Ta 8°C). TBL was negatively correlated to RQ (r2 ⫽ 0.61, P ⫽ 0.039, n ⫽ 6),
and addition of TMR or Tb did not significantly improve
the fit of the regression model. However, when RQ is
considered together with metabolic rate to estimate
protein-free rates of carbohydrate metabolism (Table
2), TBL was not significantly related to rates of carbohydrate depletion over Ta range of ⫺16 to 20°C (r2 ⫽
0.24, P ⫽ 0.27, n ⫽ 7).
DISCUSSION
Arctic ground squirrels hibernating in ambient temperatures ranging from substantially subfreezing conditions to room temperature showed changing interrelationships among Tb, TMR, and RQ that revealed
differing physiological responses to heterothermy as Tb
and requirements for thermoregulatory heat production changed. At Ta values ⬍0°C, metabolic rate increased proportionately with decreasing Ta while Tb
remained constant. At Ta values ⬎0°C, Tb increased
parallel with Ta, while TMR remained minimal and
Table 2. TMR, RQ, and TBL in arctic ground squirrels hibernating at differing Ta. Corresponding rates of
carbohydrate use are derived from RQ and TMR, assuming protein free metabolism.
Ta, °C
TMR, ml O2 䡠 g⫺1 䡠 h⫺1
RQ
Proportion of
Carbohydrate
Carbohydrate
Use, g ⫻ 106
Maximum
TBL, days
⫺16
⫺8
⫺4
0
4
8
20
0.180 ⫾ 0.008
0.089 ⫾ 0.003
0.041 ⫾ 0.004
0.016 ⫾ 0.001
0.012 ⫾ 0.000
0.012 ⫾ 0.001
0.047 ⫾ 0.006
0.86 ⫾ 0.02
0.79 ⫾ 0.01
0.77 ⫾ 0.01
0.74 ⫾ 0.02
0.70 ⫾ 0.02
0.70 ⫾ 0.02
0.88 ⫾ 0.03
0.76
0.56
0.46
0.28
0
0
0.81
163.1
60.7
22.4
5.4
0
0
45.2
6.75 ⫾ 0.62
9.44 ⫾ 0.85
13.57 ⫾ 2.26
15.01 ⫾ 0.55
13.5 ⫾ 0.94
7.67 ⫾ 1.33
5.33 ⫾ 0.33
Values are means ⫾ SE. Proportion of carbohydrate was derived from respiratory quotient (RQ), assuming metabolism of carbohydrate
(glucose) and lipid (glycerol tripalmitate) (32). Carbohydrate use is expressed per g per h. Maximum torpor bout length (TBL) was derived
from a separate group of ground squirrels kept at the corresponding ambient temperature (Ta).
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
Fig. 2. Effect of Ta on mean ⫾ SE of maximum torpor bout length in
days (TBL) of hibernating arctic ground squirrels. * Values significantly differ from TBL at Ta 0°C. N represents the number of
animals contributing to each mean.
constant until Ta and Tb increased above 12°C. These
relationships are similar to and extend those described
for other hibernating mammals held either below or
above their lower critical Ta, the Ta at which heterothermic mammals begin to defend their Tb (1, 25, 29,
51). Metabolic fuel use also changed over this range of
Ta as indicated by RQ. This uncoupling of metabolic
rate from Tb and change in sources of energy over a
wide range of Ta provides an opportunity to investigate
alternative hypotheses of what limits torpor duration
in heterothermic mammals and thus the function of
periodic arousal episodes. The lack of an overall relationship between TBL and TMR or apparent rate of
carbohydrate use does not support exclusive hypotheses related to depletion of metabolic fuels (14, 18).
Thermoregulation during torpor. The lower critical
Ta for torpid arctic ground squirrels was close to 0°C.
Although arctic ground squirrels can supercool their
abdomen to ⫺2.9°C, head and neck temperatures remain ⱖ0°C (2), which requires increased levels of heat
production at Ta ⬍0°C. As Ta decreased substantially
below 0°C, arctic ground squirrels continued steadystate torpor while increasing rates of thermogenesis. In
similar conditions, other hibernating species either
freeze (63) or return to euthermic Tb in an “alarm
arousal” (30). At Ta ⫺16°C, TMR was almost 16-fold
higher than minimum values at Ta ⬎0°C. Ta values of
⫺16°C and lower are relevant to hibernating arctic
ground squirrels. Minimum hibernacula temperatures
in burrows on the North Slope of Alaska during winter
range from ⫺18 to ⫺25°C (2, 38) and averaged ⫺8.9°C
October through April at burrow sites near where the
experimental animals were captured (9). Because the
lower critical temperature of euthermic arctic ground
squirrels is 6–10°C (11), animals overwintering in subzero burrows must be continuously thermogenic
whether they are torpid or euthermic. An animal in an
average temperature burrow of ⫺9°C without a nest
would maintain a TMR 10-fold higher than if hibernating at Ta ⬎0°C (⬃0.1 vs. 0.01 ml O2 䡠 g⫺1 䡠 h⫺1);
presence of a nest would lower this to a 6.5-fold increase in TMR and decrease lower critical temperature
of euthermic animals to near 0°C (11). These results
illustrate the substantially elevated energetic costs of
hibernating under arctic conditions encountered by
arctic ground squirrels compared with hibernators dis-
METABOLISM AND TORPOR
(47). Several hibernating species show Q10 values of
metabolic rate well above 3 during the entry phase of
torpor (23, 28, 50, 51), suggesting that temperaturedependent and -independent metabolic inhibition of
metabolism may have additive effects (36, 54). Temperature independence during steady-state torpor over
wide ranges of Tb is also apparent in hibernating alpine marmots, Marmota marmota, (1) and eastern
pygmy possums, Cercartetus nanus (51). Suppressing
TMR over this range of Tb maintains maximum energy
savings of torpor over a range of Ta values, although Ta
⬎0°C occur over only a brief part of the hibernation
season in the northern distribution of this species (9).
At higher Ta values (16–20°C), temperature-independent mechanisms are apparently overcome, thus resulting in exceptionally high Q10 values of TMR from
Ta 16 to 20°C.
Metabolic fuels of hibernation. RQ results in this
study suggest that, over an extended range of Ta,
metabolic fuel use during steady-state torpor can vary.
Hibernators are reported to use fat as the exclusive
metabolic substrate during torpor (48, 52); however,
previous researchers used a narrow range of ambient
temperatures in their investigations. An RQ value of
0.70 indicates exclusive fat catabolism and 1.0 exclusive carbohydrate catabolism. RQ values between 0.70
and 1.0 can reflect either catabolism of protein or
mixed fuel use (32). RQ of arctic ground squirrels
during torpor was positively correlated to TMR at Ta
values ⬍0°C, rising from 0.70 to 0.86 from Ta 4 to
⫺16°C, and positively correlated to Tb at Ta values
⬎8°C, rising from 0.70 to 0.88 at Ta 20°C. We do not
believe these shifts in RQ with Ta represented transitory changes in respiratory exchange, because our respirometry measurements were made on animals during steady-state conditions (constant Tb and TMR) on
the fourth day of a torpor bout, and values represent
averages over a 1-h interval. Although changes in RQ
may reflect retention or release of carbon dioxide
rather than shifts in substrate use, and resulting
changes in relative acidosis of blood have been linked
to metabolic inhibition during hibernation, these
changes occur over short time intervals (⬍16 min)
during entry into or arousal from torpor (33, 36, 43)
and therefore are unlikely to have contributed to the
differences in RQ reported here.
Why do metabolic substrates shift away from exclusively lipids at low and high Ta values? Upward shifts
in RQ during torpor likely reflect addition of carbohydrate rather than protein to the utilization of fat, since
unchanging plasma urea and nonprotein nitrogen levels suggest that protein is not catabolized during torpor (20, 44, 67) and rates of gluconeogenesis are low in
hepatocytes isolated from hibernators (21). An increase
in glucose use in arctic ground squirrels at subzero
temperatures may be related to increases in TMR
supporting thermogenesis (67). Increased carbohydrate needs would follow from elevated activity of
heart muscle, erythrocytes, and brain (all glucose-utilizing tissues) associated with supporting higher rates
of metabolism at lower Ta and, in addition and proba-
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
tributed in lower latitudes, where burrow temperatures only briefly or never decrease below freezing (1,
31, 40, 65). Arctic ground squirrels meet these thermoregulatory and energetic challenges in part through a
larger body size compared with other hibernating congeners (maximum body size 1.5 kg vs. ⬍0.6 kg in other
Spermophilus species; Refs. 9, 39), which offers S.
parryii a proportionally greater ability to store fat
combined with a lower mass specific metabolic rate and
thus an ability to fast longer than smaller species (41).
Moreover, minimum TMR in this species is among the
lowest measured in hibernating endotherms (26) and
does not begin to rise until Ta decreases ⱕ0°C. These
energetic adjustments, in addition to their ability to
supercool core body temperatures to near ⫺3.0°C, are
extreme physiological and behavioral adaptations in
an arctic resident mammal that are commensurate
with the extremes of the arctic environment.
At Ta 0°C, conductance in torpid arctic ground squirrels was minimal and similar to that in other hibernating rodents (49) and did not change as TMR increased
with decreasing Ta. In contrast, conductance increases
with increased TMR in marsupial hibernators, which
lack brown adipose tissue (BAT) and use shivering
thermogenesis at Ta less than the lower critical temperature (50, 51). Song et al. (51) suggest that, in
marsupials, increased conductance during shivering is
due to increased peripheral circulation. Rodents rely
on nonshivering thermogenesis during hibernation
and are not known to shiver during steady-state torpor; therefore, different patterns of conductance with
respect to Ta may be related to the different mechanisms of thermogenesis in rodent and marsupial hibernators.
At Ta ⬎0°C, thermoregulatory heat production was
absent, as indicated by minimum TMR and ⌬T, and
heat loss was facilitated by conductance that significantly increased compared with subfreezing temperatures. Values for conductance calculated for torpid arctic ground squirrels without a nest at Ta 0 and 4°C
were lower by 64 and 55%, respectively, than values
predicted by Snyder and Nestler (49), based on measures of TMR of smaller animals hibernating at Ta 6°C.
The lower than predicted conductance could be explained by the larger animals used in this study (⬃200
g greater mass) and greater insulative properties of the
fur.
TMR of arctic ground squirrels was minimal at Ta
4–12°C and did not significantly increase until Ta and
Tb were ⱖ16°C (Fig. 1); thus a thermal neutral zone
between Ta 0 and 16°C exists for torpid arctic ground
squirrels. TMR remained constant over this range despite the passive increase in Tb with Ta, averaging
0.67°C greater than Ta, indicating that hibernating
arctic ground squirrels use temperature-independent
mechanisms of metabolic inhibition. Although the
overall increase in TMR from Ta 4 to 20°C is represented by a Q10 of 2.4, Q10 across these Ta values
ranges from 1.0 (Ta 4–8°C) to 14.1 (Ta 16–20°C; Table
1). Temperature effects on tissue and whole organism
rates of metabolism normally have Q10 values of 2–3
R259
R260
METABOLISM AND TORPOR
water (16) or urea (45), may accumulate during torpor
when kidney filtration and liver function are diminished or absent (15), and hibernators must arouse to
remove them. Metabolism-linked hypotheses assume
that the rate of depletion or accumulation of the critical
substance(s) is proportional to the metabolic rate during torpor. Although there is some experimental evidence supporting specific aspects of these hypotheses
in individual species, no consensus has been reached
for acceptance of the general metabolic rate hypothesis
(23, 24, 62). Body temperature hypotheses alternatively center on low tissue temperature inhibition of
other homeostatically regulated processes that are not
directly linked to metabolic rate. For example, hibernators with cold brains may not be able to sleep, yet
sleep debt could continue to accumulate during torpor,
albeit at a reduced rate (13, 57). Hibernators may be
forced to warm periodically to maintain sleep balance
(4, but see Refs. 34, 55). Other body temperature hypotheses specify a requirement for periodic high brain
temperatures for memory consolidation or maintenance (42, 56), for preservation of neuronal connections
in the central nervous system (34, 46, 55), a need of
high Tb for maintenance of opiate system suppression
of metabolism (61), for reproductive development (3),
or a requirement of high tissue temperatures for gene
expression, e.g., transcription or translation, and
thereby a generalized need for periodic euthermia for
homeostasis of gene products such as mRNA or proteins (37). These hypotheses assume that the need for
arousals develops at a rate proportional to body or
brain temperature during hibernation, but not necessarily in proportion to whole body metabolic rate.
The changes in TBL found in the present study offer
support for both the metabolic rate and body temperature hypotheses, depending on whether Ta is above or
below 0°C, but overall we hypothesize TBL in arctic
ground squirrels depends on brain temperature. At Ta
⬍0°C, TBL decreases concomitantly with increasing
rates of metabolism, which is consistent with the metabolic hypotheses (25). The general reciprocal relationship between changing RQ and TBL across the full
range of Ta supports the specific hypothesis that depletion of nonlipid fuels, e.g., glucose, limits how long
torpor can be sustained before an arousal is required
(20). However, the observed decrease in TBL at Ta
⬎0°C, when TMR and estimated rates of glucose metabolism remain minimal, is not consistent with the
metabolic hypothesis.
The reciprocal decrease of TBL with increasing Ta
and Tb above 0°C (Fig. 2), which has been experimentally demonstrated in arctic ground squirrels to be
linked to Ta and not to season (5) and is similar in other
hibernating mammals (25, 58), is most supportive of
the body temperature hypotheses, whereas the decrease in TBL at Ta ⬍0°C while Tb remains relatively
constant is not.
Arousal episodes may serve alternative functions as
Tb and requirements for thermoregulation vary. Thus
arctic ground squirrels may arouse more frequently at
Ta ⬍0°C to replenish glycogen stores and more fre-
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
bly most significantly, glucose requirements to support
increased nonshivering thermogenesis in BAT (12, 27).
BAT mass increases three- to fourfold in arctic ground
squirrels before hibernation, through hypertrophy and
hyperplasia (7), and, in rats, glucose uptake by BAT
increases 50- to 100-fold after cold exposure or norepinephrine injection (35, 59). Increased glucose uptake in
thermogenic BAT supplies oxaloacetate (via conversion
to pyruvate) during citrate acid cycle oxidation (10).
Glucose utilization during torpor is indicated by progressive decreases in blood glucose and liver glycogen
concentrations over the torpor bout, which are replenished during arousal episodes (18, 20). Much of this
replacement carbohydrate may be derived from protein
in arctic ground squirrels, which lose 30–40% of their
lean body mass over the hibernation season (8, 19).
Gluconeogenesis from amino acids is required because
glycerol release from the metabolism of triacylglycerols
is insufficient to provide for glucose requirements during torpor when metabolic rates are low. Zimmerman
(67) estimated that TMR of arctic ground squirrels
would have to reach 0.2 ml O2 䡠 g⫺1 䡠 h⫺1 of only fat
oxidation for gluconeogenesis from glycerol to prevent
depletion of glycogen. TMR this high would be reached
at Ta of approximately ⫺20°C (Fig. 1). These temperatures do occur in hibernacula of arctic ground squirrels, but they are not sustained for long intervals (9),
suggesting an additional need for gluconeogenesis from
muscle tissue over the majority of the hibernation
season. Nonetheless, higher rates of glycerol release
and its combustion as carbohydrate may contribute to
the upward shift of RQ as TMR increases at lower Ta
values.
These arguments for an increase in RQ at Ta values
⬍0°C cannot altogether explain its increase at Ta values ⬎8°C. At Ta 12°C, RQ was significantly higher
compared with Ta at 4–8°C, without a concomitant
increase in TMR and thermogenesis. In addition, overall increases in RQ and TMR at Ta values ⬎0°C are not
proportional to changes at Ta ⬍0°C. At Ta values ⬎8°C,
RQ is most directly related to changes in Tb, suggesting
a changing use of metabolic fuels as tissue temperatures rise, but for unknown reasons.
TBL and the function of arousal episodes. The changing relationships among Ta, Tb, TMR, and the use of
metabolic fuels in hibernating arctic ground squirrels
provides an opportunity to examine alternative hypotheses of what limits duration of torpor in mammals
and thus the functional significance of arousal episodes. The many hypotheses for the physiological function of arousal episodes fall into two general categories:
metabolic rate and body temperature. Metabolic rate
hypotheses associate arousals with a requirement of
high Tb for reestablishing homeostasis of some metabolism-linked process that goes awry at low Tb (17, 23).
For example, metabolic fuels used for maintenance
metabolism, e.g., glucose (20) or fatty acids (14), may
be depleted during torpor due to low temperature inhibition of enzymes linked to their release or synthesis,
requiring arousals for their replenishment in the blood
and tissues. Alternatively, metabolic by-products, e.g.,
METABOLISM AND TORPOR
We thank Andrée Porchet and Sharon Loy for help with animals,
Brett Luick for design and software for respirometry measures, and
Øivind Tøien and Alison York for reading the manuscript.
This study was funded by grants from the University of Alaska’s
Center for Global Change and Arctic System Science and the American Heart Association (to C. L. Buck) as well as by National Science
Foundation Grant OPP-9819540 (to B. M. Barnes).
13.
14.
15.
16.
17.
18.
19.
20.
21.
REFERENCES
1. Arnold W, Heldmaier G, Ortmann S, Pohl H, Ruf T, and
Steinlechner S. Ambient temperatures in hibernacula and
their energetic consequences for alpine marmots (Marmota marmota). J Therm Biol 16: 223–226, 1991.
2. Barnes BM. Freeze avoidance in a mammal: body temperatures
below 0°C in an Arctic hibernator. Science 244: 1521–1616, 1989.
3. Barnes BM, Kretzmann M, Licht P, and Zucker I. Reproductive development in hibernating ground squirrels. In: Living
in the Cold: Physiological and Biochemical Adaptations, edited
by Heller HC, Musacchia XJ, and Wang LCH. New York:
Elsevier, 1986, p. 245–251.
4. Barnes BM, Omtzigt C, and Daan S. Hibernators periodically
arouse to sleep. In: Life in the Cold Ecological, Physiological, and
Molecular Mechanisms, edited by Carey C, Florant GL, Wunder
BA, and Horwitz B. Boulder, CO: Westview, 1993, p. 556–558.
5. Barnes BM and Ritter D. Patterns of body temperature
change in hibernating arctic ground squirrels. In: Life in the
Cold: Ecological, Physiological, and Molecular Mechanisms, edited by Carey C, Florant GL, Wunder BA, and Horwitz B.
Boulder, CO: Westview, 1993, p.120–130.
6. Boyer BB and Barnes BM. Molecular and metabolic aspects of
mammalian hibernation. Bioscience 49: 713–724, 1999.
7. Boyer BB, Barnes BM, Kopecky J, Jacobson A, and Hermanska J. Molecular control of prehibernation brown fat
growth in arctic ground squirrels. In: Living in the Cold: Ecological, Physiological, and Molecular Mechanisms, edited by Carey
C, Florant GL, Wunder BA, and Horwitz B. Boulder, CO: Westview, 1993, p. 483–491.
8. Buck CL and Barnes BM. Annual cycle of body composition
and hibernation in free-living arctic ground squirrels. J Mammal
80: 430–442, 1999.
9. Buck CL and Barnes BM. Temperatures of hibernacula and
changes in body composition of arctic ground squirrels over
winter. J Mammal 80: 1264–1276, 1999.
10. Cannon B and Nedergaard J. Energy dissipation in brown
fat. Experientia Suppl 32: 107–111, 1978.
11. Chappell MA. Standard operative temperatures and cost of
thermoregulation in the arctic ground squirrel, Spermophilus
undulatus. Oecologia (Berl) 49: 397–403, 1981.
12. Cooney G, Curi RMA, Newsholme P, Simpson M, and
Newsholme EA. Activities of some key enzymes of carbohy-
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
drate, ketone body, adenosine and glutamate metabolism in
liver, and brown and white adipose tissues of the rat. Biochem
Biophys Res Commun 138: 687–692, 1986.
Daan S, Barnes BM, and Strijkstra AM. Warming up for
sleep? Ground squirrels sleep during arousals from hibernation.
Neurosci Lett 128: 265–268, 1991.
Dark J and Ruby NF. Metabolic fuel utilization during hibernation. In: Life in the Cold: Ecological, Physiological, and Molecular Mechanisms, edited by Carey C, Florant GL, Wunder BA,
and Horwitz B. Boulder, CO: Westview. 1993, p. 167–174.
Deavers DR and Musacchia WJ. Water metabolism and renal
function during hibernation and hypothermia. Federation Proc
39: 2969–2973, 1980.
Fisher KC and Mannery JF. Water and electrolyte metabolism in heterotherms. In: Mammalian Hibernation III, edited by
Fisher KC, Dawe AP, Lyman CP, Schönbaum E, and South FE,
Jr. New York: Elsevier, 1967, p. 235–279.
French AR. Allometries of the duration of torpid and euthermic
intervals during mammalian hibernation: a test of the theory of
metabolic control of the timing of changes in body temperature.
J Comp Physiol [B] 156: 13–19, 1985.
Galster WA and Morrison P. Cyclic changes in carbohydrate
concentrations during hibernation in the arctic ground squirrel.
Am J Physiol 218: 1228–1232, 1970.
Galster WA and Morrison P. Seasonal changes in body composition of the arctic ground squirrel, Citellus undulatus. Can J
Zool 54: 74–78, 1976.
Galster WA and Morrison PR. Gluconeogenesis in arctic
ground squirrels between periods of hibernation. Am J Physiol
228: 325–330, 1975.
Gehnrich SC and Aprille JR. Hepatic gluconeogenesis and
mitochondrial function during hibernation. Comp Biochem
Physiol B Biochem 91: 11–16, 1988.
Geiser F. Reduction of metabolism during hibernation and
torpor in mammals and birds: temperature effect of physiological
inhibition? J Comp Physiol [B] 158: 25–37, 1988.
Geiser F. Metabolic rate reduction during hibernation. In: Life
in the Cold: Ecological, Physiological, and Molecular Mechanisms, edited by Carey C, Florant GL, Wunder BA, and Horwitz
B. Boulder, CO: Westview, 1993, p. 549–554.
Geiser F and Broome LS. The effect of temperature on the
pattern of torpor in a marsupial hibernator. J Comp Physiol [B]
163: 133–137, 1993.
Geiser F and Kenagy GJ. Torpor duration in relation to
temperature and metabolism in hibernating ground squirrels.
Physiol Zool 61: 442–449, 1988.
Geiser F and Ruf T. Invited perspectives in physiological
zoology: hibernation versus daily torpor in mammals and birds:
physiological variables and classification of torpor patterns.
Physiol Zool 68: 935–966, 1995.
Gibbons JM, Denton RM, and McCormack JG. Evidence
that noradrenaline increases pyruvate dehydrogenase activity
and decreases acetyl-CoA carboxylase activity in rat intrascapular brown adipose tissue in vivo. Biochem J 228: 751–755, 1985.
Heldmaier G and Ruf T. Body temperature and metabolic rate
during natural hypothermia in endotherms. J Comp Physiol [B]
162: 696–706, 1992.
Heller HC and Colliver GW. CNS regulation of body temperature during hibernation. Am J Physiol 227: 583–589, 1974.
Heller HC and Hammel HT. CNS control of body temperature
during hibernation. Comp Biochem Physiol A Physiol 41: 349–
359, 1972.
Kenagy GJ, Sharbaugh SM, and Nagy KA. Annual cycle of
energy and time expenditure in a golden-mantled ground squirrel population. Oecologia (Berl) 78: 269–282, 1989.
Kleiber M. The Fire of Life: An Introduction to Animal Energetics. Malabar, FL: Krieger, 1975.
Krilowitz BL. Ketone body metabolism in a ground squirrel
during hibernation and fasting. Am J Physiol Regulatory Integrative Comp Physiol 249: R462–R470, 1985.
Larkin JE and Heller HC. Sleep after arousal from hibernation is not homeostatically regulated. Am J Physiol Regulatory
Integrative Comp Physiol 276: R522–R529, 1999.
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
quently at Ta ⬎0°C to maintain brain functions. A
singular correlate to TBL may still be hypothesized,
however, if regional heterothermy occurs in hibernators at Ta ⬍0°C. A 2–3°C difference between core and
neck temperatures occurs in torpid arctic ground squirrels at Ta ⫺4.3°C (2). This is likely due to the anterior
location (subscapular and periarterial) of the largest
stores of BAT, which are the major thermogenic tissues
maintaining gradients between Tb and subzero Ta.
This regional heterothermy may increase as Ta decreases and the requirement for thermogenesis increases. An increase in heterothermy at Ta ⫺16°C
resulting in Tb of 0°C but brain temperatures near
10°C would result in TBL equivalent to Ta of 10°C,
when brain temperatures are also near 10°C. Resolving causal relationships between brain temperature
and TBL should be amenable to experiments that vary
brain temperature separately from Tb and metabolic
rate (30).
R261
R262
METABOLISM AND TORPOR
51. Song X, Kortner G, and Geiser F. Thermal relations of metabolic rate reduction in a hibernating marsupial. Am J Physiol
Regulatory Integrative Comp Physiol 273: R2097–R2104, 1997.
52. South FE and House WA. Energy metabolism in hibernation.
In: Mammalian Hibernation III, edited by Fisher KC, Dawe AP,
Lyman CP, Schönbaum E, and South FE Jr. New York: Elsevier,
1967, p. 305–324.
53. Storey KB. Metabolic regulation in mammalian hibernation:
enzyme and protein adaptations. Comp Biochem Physiol A
Physiol 118: 1115–1124, 1997.
54. Storey KB and Storey JB. Metabolic rate depression and
biochemical adaptation in anaerobiosis, hibernation and estivation. Q Rev Biol 65: 145–174, 1990.
55. Strijkstra AM and Daan S. Dissimilarity of slow-wave activity
enhancement by torpor and sleep deprivation in a hibernator.
Am J Physiol Regulatory Integrative Comp Physiol 275: R1110–
R1117, 1998.
56. Strumwasser F, Gilliam JJ, and Smith JL. Long term studies on individual hibernating animals. Bull Mus Comp Zool
124:285–320, 1964.
57. Trachsel L, Edgar DM, and Heller HC. Are ground squirrels
sleep deprived during hibernation? Am J Physiol Regulatory
Integrative Comp Physiol 260: R1123–R1129, 1991.
58. Twente JW and Twente JA. Effects of core temperature upon
duration of hibernation of Citellus lateralis. J Appl Physiol 20:
411–416, 1965.
59. Vallerand AL, Pérusse F, and Bukowiecki LJ. Stimulatory
effects of cold exposure and cold acclimation on glucose uptake in
rat peripheral tissues. Am J Physiol Regulatory Integrative
Comp Physiol 259: R1043–R1049, 1990.
60. Wang LCH. Time patterns and metabolic rates of natural torpor
in the Richardson’s ground squirrel. Can J Zool 57: 149–155,
1979.
61. Wang LCH. Neurochemical regulation of arousal from hibernation. In: Life in the Cold: Ecological, Physiological, and
Molecular Mechanisms, edited by Carey C, Florant GL,
Wunder BA, and Horwitz B. Boulder, CO; Westview, 1993, p.
559–561.
62. Willis LS. The mystery of the periodic arousal. In: Hibernation
and Torpor in Mammals and Birds, edited by Lyman CP, Willis
JS, Malan A, and Wang LCH. New York: Academic, 1982, p.
92–101.
63. Wit LC and Twente JW. Metabolic responses of hibernating
golden-mantled ground squirrels Citellus lateralis to lowered
environmental temperatures. Comp Biochem Physiol A Physiol
74: 823–827, 1983.
64. Withers PC. Measurement of VO2, VCO2, and evaporative water
loss with a flow-through mask. J Appl Physiol 42: 120 –123,
1977.
65. Young PJ. Hibernating patterns of free-ranging Columbian
ground squirrels. Oecologia (Berl) 83: 504–511, 1990.
66. Zar JH. Biostatistical Analysis. Englewood Cliffs, NJ: PrenticeHall, 1984.
67. Zimmerman ML. Carbohydrate and torpor duration in hibernating golden-mantled ground squirrels (Citellus lateralis).
J Comp Physiol [B] 147: 129–135, 1982.
Downloaded from http://ajpregu.physiology.org/ by 10.220.33.3 on October 1, 2016
35. Liu X, Pérruse F, and Bukowiecki LJ. Chronic norepinephrine infusion stimulates glucose uptake in white and brown
adipose tissues. Am J Physiol Regulatory Integrative Comp
Physiol 266: R914–R920, 1994.
36. Malan A. pH as a control factor in hibernation. In: Living in the
Cold: Physiological and Biochemical Adaptations, edited by
Heller HC, Musacchia XJ, and Wang LCH. New York: Elsevier,
1986, p. 61–70.
37. Martin SL, Srere HK, Belke D, Wang LCH, and Carey HV.
Differential gene expression in the liver during hibernation in
ground squirrels. In: Life in the Cold: Ecological, Physiological,
and Molecular Mechanisms, edited by Carey C, Florant GL,
Wunder BA, and Horwitz B. Boulder, CO: Westview, 1993, p.
443–453.
38. Mayer WV. The protective value of the burrow system to the
hibernating arctic ground squirrel, Spermophilus undulatus.
Anat Rec 122: 437–438, 1955.
39. Michener GR. Age, sex, and species differences in the annual
cycles of ground-dwelling sciurids: implication for sociality. In:
The Biology of Ground Dwelling Squirrels: Annual Cycles, Behavioral Ecology, and Sociality, edited by Murie JO and
Michener GR. Lincoln: Univ. of Nebraska Press, 1984, p. 81–
107.
40. Michener GR. Sexual differences in over-winter torpor patterns of Richardson’s ground squirrels in natural hibernacula.
Oecologia (Berl) 89: 397–406, 1992.
41. Morrison PR. Some interrelations between weight and hibernation function. Bull Mus Comp Zool 124: 75–91, 1960.
42. Mrosovsky N. Hibernation and the Hypothalamus. New York:
Appleton-Century-Crofts, 1971.
43. Nestler JR. Relationships between respiratory quotient and
metabolic rate during entry to and arousal from daily torpor in
deer mice (Peromyscus maniculatus). Physiol Zool 63: 504–515,
1990.
44. Pengelley ET, Asmundson SJ, and Uhlman C. Homeostasis
during hibernation in the golden-mantled ground squirrel, Citellus lateralis. Comp Biochem Physiol A Physiol 38: 645–653,
1971.
45. Pengelley ET and Fisher KC. Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis
tescorum. Can J Zool 39: 105–120, 1961.
46. Popov VI and Bocharova LS. Hibernation-induced structural
changes in synaptic contacts between mossy fibers and hippocampal neurons. Neuroscience 48: 53–62, 1992.
47. Roberts JC and Smith RE. Effects of hibernation on metabolic
rates of liver and brown fat homogenates. Can J Biochem 45:
1763–1771, 1967.
48. Snapp BD and Heller HC. Suppression of metabolism during
hibernation in ground squirrels (Citellus lateralis). Physiol Zool
54: 297–307, 1981.
49. Snyder GK and Nestler JR. Relationships between body temperature, thermal conductance, Q10 and energy metabolism during daily torpor and hibernation in rodents. J Comp Physiol [B]
159: 667–675, 1990.
50. Song X, Kortner F, and Geiser F. Reduction of metabolic rate
and thermoregulation during daily torpor. J Comp Physiol [B]
165: 291–297, 1995.