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1 German Institute of Human Nutrition, D-14558 Bergholz-Rehbrücke; and 2 Philipps University, D-35032 Marburg, Germany
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Body temperature and
metabolic rate were recorded continuously in two groups of marmots
either exposed to seasonally decreasing ambient temperature (15 to
0°C) over the entire hibernation season or to short-duration
temperature changes during midwinter. Hibernation bouts were
characterized by an initial 95% reduction of metabolic rate
facilitating the drop in body temperature and by rhythmic fluctuations
during continued hibernation. During midwinter, we observed a constant
minimal metabolic rate of 13.6 ml
O2 · kg
1 · h1
between 5 and 15°C ambient temperature, although body temperature increased from 7.8 to 17.6°C, and a proportional increase of
metabolic rate below 5°C ambient temperature. This apparent lack of
a Q10 effect shows that energy
expenditure is actively downregulated and controlled at a minimum level
despite changes in body temperature. However, thermal conductance
stayed minimal (7.65 ± 1.95 ml
O2 · kg1 · h1 · °C1)
at all temperatures, thus slowing down cooling velocity when entering
hibernation. Basal metabolic rate of summer-active marmots was double
that of winter-fasting marmots (370 vs. 190 ml
O2 · kg1 · h1).
In summary, we provide strong evidence that hibernation is not only a
voluntary but a well-regulated strategy to counter food shortage and
increased energy demands during winter.
thermal conductance; metabolic rate; body temperature-ambient temperature gradient; thermoregulation; hibernation physiology
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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ALPINE MARMOTS (Marmota marmota) overcome the problems of poor food availability and severe environmental conditions during winter by the means of deep hibernation. Toward the end of September, they cease all above-ground activity and retreat into their protected hibernacula where they experience a continuous decrease of ambient temperature (Ta) from 12 to 15°C in autumn to ~0°C in spring (4). They end the hibernation season early in April and thus spend >6 mo in their hibernacula. During prolonged bouts of hibernation, metabolic rate (MR) is reduced to a fraction of the euthermic level, and body temperature (Tb) is close to Ta (13, 28). Thermoregulation continues in deep hibernation like in several species of hibernators or torpor-exhibiting species (7, 11, 16, 17), but unlike various ground squirrels, which exhibit Tb values near or below the freezing point (5), Alpine marmots always control their Tb at values above 3-5°C (3, 4).
Marmots rely exclusively on body fat reserves to fuel all energy demands during hibernation. Therefore, the reduction of MR in deep hibernation is of vital energetic significance during the long winter season. Although low MR and Tb values are described in many species, the mechanisms and physiological control of metabolic reduction are only poorly understood and remain controversial (8, 9, 13-15, 25, 26, 32, 33). Alpine marmots are well known as hibernators and were one of the first species in which physiological changes in hibernation were measured (6). However, there is only poor knowledge concerning the regulation of Tb and energy requirements during hibernation as well as in the normothermic state. We therefore continuously measured Tb and MR of marmots during the entire hibernation season. One group of adult Alpine marmots hibernated under seasonally decreasing Ta conditions, and MR and Tb were recorded continuously to obtain the entire spectrum of Tb and MR changes. A second group of marmots was exposed to different Ta values during midwinter, when hibernation bouts are longest (1, 13), to analyze their potential for Tb and MR regulation in deep hibernation.
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MATERIALS AND METHODS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Animal Maintenance
Alpine marmots were either bred in our breeding colony in Philipps University Marburg or in Hellabrunn Zoo Munich. The latter were bought as juveniles and were raised under natural climatic conditions and the photoperiod of Marburg (50°49 N, 09 E). During the summer, marmots were kept in family groups in outdoor enclosures provided with artificial burrows and were fed one time per day with green grass and herbs and with a mixture of corn, seed, and rabbit chow (Altromin). A few weeks before the start of the experiments, marmots were provided with precalibrated temperature transmitters (Kronwitter TWS; Oberpframmern or Minimitter, Sunriver, OR). These transmitters allow long-term records of Tb and were surgically implanted in the abdominal cavity under deep Ketanest/Rompun anesthesia. With the onset of the hibernation season (October), marmots were transferred to climate chambers where they stayed in constant darkness until spring.Experiments and Techniques
Experiment I: hibernation pattern and energy requirements of Alpine marmots under seasonally decreasing temperature conditions. One male and two female adult marmots were housed individually in closed Perspex boxes of 2.6 l volume each. The Perspex boxes were provided with a thin layer of hay and served as metabolic cages. The marmots had no additional nesting material and remained without food or water from October 15th until the end of the hibernation season, i.e., March 5th. Ta within the climate chamber was measured with a thermocouple attached to the inside wall of the Perspex box. Ta was decreased gradually in steps of 2°C from 15°C in October to 0°C in March but remained constant at a given temperature until each individual showed at least two complete hibernation bouts. Tb and MR were recorded continuously throughout the entire hibernation season.Experiment II: regulation of Tb and
metabolic heat production in hibernating and normothermic marmots.
Four male and four female adult Alpine marmots hibernated undisturbed
at 7°C Ta until midwinter.
They were housed in two groups in wooden nest boxes containing hay as
nesting material. During January and February, individual animals were
transferred to closed Perspex boxes (as in experiment I). After
they reentered deep hibernation,
Ta was either increased stepwise
from 7 to 15°C or decreased to 
0.5°C. Each step lasted
at least 24 h, and Tb (5 marmots)
and MR (up to 8 marmots) were recorded continuously.
5°C. Each
Ta step lasted until MR
established a constant resting level, but each lasted at least 1 h.
Techniques.
Tb was recorded in 6-min intervals
using a computerized recording system. For metabolic measurements, air
flow through the metabolic boxes was monitored by mass flow meters (Tylan) and was controlled at 40-50 l/h when marmots were
hibernating and 400 l/h during normothermia. The air was dried with
silica gel and was analyzed for its
O2 and
CO2 content with an
O2 analyzer (Oxytest S; Hartmann & Braun) and a CO2 analyzer (URAS
2T; Hartmann & Braun). Both are two-channel analyzers comparing sample
air from the animal boxes with reference air from the climate chamber. They have a measuring range of 20-21 vol/100 vol
O2, 0-1 vol/100 vol
CO2, and 0.001 vol/100 vol
resolution. The climate chamber was continuously supplied with outside
air. A magnetic valve system allowed the measurement of six channels in
sequence. The setup admitted continuous records of
Tb,
Ta, and MR in 6-min intervals for
each individual. To prevent marmots from dehydration during hibernation, the surrounding air was humidified.
For measurements of normothermic marmots, individual animals were
transferred to Perspex boxes and placed in a climate chamber (500 SD;
Weiss). MR was determined as described above but was recorded in 1-min intervals.
MR was calculated according to the equation
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Statistical Analysis
Results are given as means ± SE. Data obtained from the same individual at the same Ta were averaged for statistical analysis. "N" is the number of animals, and "n" is the total number of measurements. Differences between means were examined using a Student's t-test. Regressions were determined by the methods of least squares.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Experiment I: Hibernation Pattern and Energy Requirements of Alpine Marmots Under Seasonally Decreasing Temperature Conditions
Body weight. Body weight decreased during winter from 3,870 ± 138 g (n = 3) in autumn to 2,750 ± 144 g in spring, i.e., marmots lost 1,253 ± 111 g body mass or 32.5 ± 2.5% of the prehibernation mass (PHM). The absolute daily mass loss was 12.8 ± 0.05 g/day, and the weight-specific daily mass loss was 0.33 ± 0.02% PHM/day.Hibernation bout characteristics.
Figure 1 shows the
Tb course of an Alpine marmot over
the entire hibernation season in the laboratory, beginning in early
November at ~15°C Ta. Bouts
of continuous hibernation were periodically interrupted by short phases
of normothermia. Tb in deep
hibernation was adjusted to the progressively decreasing
Ta, and hibernation bouts lasted longer (e.g., up to 141 h at Ta
7°C). Nevertheless, below a certain Ta threshold of ~5°C, a
minimum Tb was maintained constant
despite the further drop of Ta,
and bout length was shortened (up to 41 h at
Ta 2.5°C). Mean minimum
Tb of this particular marmot was ~9.5°C at 5°C Ta.
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Figure 2 shows the time course of MR and
Tb of a hibernating Alpine marmot
over a time period of 13 days. Ta
within the climate chamber was ~7°C at the end of December and
the beginning of January and was decreased to 2.5°C in
mid-February. Each hibernation episode was initiated by a rapid
decrease in MR from the normothermic to the torpid level, and minimum
values of MR below 20 ml
O2 · kg1 · h1
were reached after ~10 h. This initial metabolic suppression (MRinit) was followed by a
slightly elevated level of MR when hibernation progressed until the
next arousal occurred. Tb
decreased rapidly with the onset of the hibernation bout and continued
to decrease through the entire bout. During continued hibernation, marmots maintained a minimum MR
(MRmin) that was periodically interrupted by bursts of heat production. These bursts became more
pronounced with increasing cold load (Fig.
3) and reached or even exceeded
normothermic resting MR at or below
Ta 2.5°C, whereas burst
frequency remained constant with 13.02 ± 0.48 bursts/day at any
Ta. For estimating the true energy
costs of a hibernating marmot at a given
Ta, we therefore calculated an
average hibernation MR (MRhib)
that includes MRmin and the
metabolic bursts.
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Minimum Tb (Fig.
4A)
during hibernation was adjusted to
Ta within certain limits and
decreased in parallel with the decline in
Ta. When
Ta was lowered below 7°C,
Tb was regulated at a level of
~10-11°C. Consequently, the
Tb-Ta
gradient rose with the drop in Ta,
and marmots increased their mean
MRhib to defend their preferred
hibernation Tb (Fig.
4B). This metabolic response
occurred proportionally to the additional cold load and reached highest values of ~400 ml O2/h at
Ta = 0°C. At
Ta, values above 11°C
MRhib remained constant at ~100
ml O2/h, irrespective of the
increase of Tb from 13.6°C at
11°C Ta to 18.2°C at
15°C Ta. We observed a
comparable pattern for the dependency of
MRmin on
Ta, but on a lower level and with
a gentle slope (Table 1). However, we observed no significant increase in
MRinit with decreasing
Ta.
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The expression of MR in weight-specific units revealed a comparable relationship of MR with Ta (Fig. 4C) with one exception. Two of three marmots exhibited a significant increase of MRinit with decreasing Ta, whereas the third marmot showed no dependency of MRinit on Ta (Table 1).
Experiment II: Regulation of Tb and Metabolic Heat Production in Hibernating and Normothermic Marmots
Body weight. Mean body weight of Alpine marmots was 3,090 ± 157 g (n = 8) during hibernation, 3,358 ± 75 g (n = 6) during normothermia in winter, and 3,599 ± 64 g (n = 9) in summer. Body weight was not different between winter hibernation and winter normothermia but differed significantly between both hibernation and summer normothermia (P < 0.01) and winter normothermia and summer normothermia (P < 0.05).The range of Ta in which Alpine
marmots entered deep hibernation ranged from 0.5 to 16°C in
the laboratory during midwinter. Any temperatures exceeding these
threshold levels induced an immediate arousal from hibernation.
Tb (Fig.
5) was closely adjusted to
Ta between 5 and 15°C
Ta, and we observed a
Tb-Ta
gradient of 1-3°C. Because
Tb followed Ta, an increase in
Tb from 7.8°C at 5°C
Ta to 17.6°C at 15°C
Ta could be recorded. Below
5°C Ta,
Tb was maintained more or less stable, but minimal metabolic heat production increased proportionally with decreasing Ta to a maximum of
50 ml
O2 · kg1 · h1.
Between 5 and 15°C Ta, MR
remained constant at 13.6 ± 0.55 ml O2 · kg1 · h1.
At 16°C Ta,
Tb and MR were elevated again,
marmots regulated their Tb at
~4.7°C above Ta, and heat
production rose to 23.5 ± 2.43 ml
O2 · kg1 · h1.
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Thermal conductance was established at a minimal level of 7.65 ± 1.95 ml
O2 · kg1 · h1 · °C1.
Conductance did not change with Ta
but remained constant below and above 5°C
Ta.
Nevertheless, despite the pronounced increase of energy demands in the
cold, hibernation MR remained a fraction of normothermic resting MR
(MRnorm) at any given
Ta (Fig.
6). A drop in
Ta from 30 to 5°C
during winter caused a >2.5-fold rise in
MRnorm from 190 ml
O2 · kg1 · h1
between 15 and 25°C Ta to 490 ml
O2 · kg1 · h1
at 5°C Ta. The true
reduction of energy costs by hibernation increased from ~250 ml
O2 · kg1 · h1
at 15°C Ta to 400 ml
O2 · kg1 · h1
at 0°C Ta.
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The whole extent of energy reduction by the means of hibernation becomes even more pronounced when MRmin is compared with MRnorm during summer. Summer-active marmots exhibit a higher weight-specific MR at any given Ta, and basal MR is doubled compared with fasting marmots during winter. Moreover, the start of the linear increase of MR with decreasing Ta, i.e., the lower critical temperature (Tlc), is shifted to lower Ta values (15 vs. 20°C). However, the slope of the regression line calculated from values below Tlc does not differ between winter and summer normothermic marmots.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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Hibernation is a voluntary and well-regulated adaptive response to
conditions of low Ta and food
shortage that occur during winter. The results of our study clearly
demonstrate that entrance into hibernation is facilitated by an initial
maximum suppression of metabolic heat production to values even below
10 ml
O2 · kg1 · h1.
The transition to this level of reduced metabolism requires ~10 h,
and it is maintained for around 1 day. Due to the shut off of heat
production, Tb starts to decline
and continues its decline throughout the entire hibernation bout.
Minimum Tb is generally reached
after several days and just before arousal. The decline in
Tb is very regular and smooth,
indicating that the threshold of counteractive metabolic heat
production is always adjusted just below the actual
Tb, which is consistent with the sliding set point for Tb during
entrance into hibernation proposed by Heller et al. (18). Metabolic
reduction always precedes the drop in
Tb, and it is evident that
hypometabolism is the cause of hypothermia and not its result. This
finding is not unique in Alpine marmots and has been demonstrated in
true hibernators like woodchucks (23), golden hamsters (22), and
golden-mantled ground squirrels (15) as well as in torpor-exhibiting
species like Djungarian hamsters (14) and lemurs (29).
During continued hibernation, MR is slightly elevated and is frequently interrupted by bursts of heat production. This pattern of MR control was rather unexpected but clearly demonstrates continuation of active regulation of metabolism, even in deep hibernation. Regular fluctuations of MR during hibernation have previously been recorded (10, 34), but they occurred in much shorter intervals with an amplitude well below resting MR. At high Ta values (11-15°C Ta), metabolic bursts in marmots were rather small but increased in amplitude with increasing cold load. At Ta values at and below 2.5°C, the amplitude of these bursts reached or even exceeded normothermic resting MR at that Ta, as shown in Figs. 2 and 3. This finding is especially remarkable as this particular marmot hibernated at ~12°C Tb.
It has been shown that species displaying hibernation or torpor can elevate their heat production at low Ta values to defend a minimal Tb, but the results of this study demonstrate that marmots defend their minimal Tb with patterned pulsatile increases in metabolism. Additional cold load evokes a proportional increase of MRmin (Fig. 4 and Table 1) and a major increase in burst amplitude. The latter results in a proportional but steeper rise of MRhib with decreasing Ta compared with MRmin (Table 1). An alternative strategy to the rise in amplitude would be to increase burst frequency in the cold, but we found no indication that marmots make use of this mechanism. On the contrary, we counted a constant number of metabolic burst per day (13.02 ± 0.48 bursts/day) irrespective of the change in Ta.
It is generally accepted that the ability for thermoregulation persists
during that part of the hibernation process when
Tb reaches the set point of
metabolic defense (16, 17, 19, 22, 24, 36), and it seems reasonable
that the physiological processes underlying thermoregulation at low
Ta values during hibernation,
torpor, and normothermia are similar (14, 20, 32). At
Ta values above the
Tb set point, i.e., above the
animal's preferred Tb, there is
no need for counteractive heat production. Tb passively followed changes in
Ta, and minimal MR stabilized at a
plateau of 13.6 ± 0.55 ml
O2 · kg1 · h1
over a wide range of Tb. This
stability of heat production has previously only been described for
hibernating ground squirrels (15), and it contradicts expected
temperature effects on MR. Furthermore, it suggests an active control
of MR at a minimum rate independent from
Tb. Otherwise, we would expect an
increase in MR with increasing Tb,
i.e., a Q10 within the range of
two to three, which is "normal" for in vitro systems (27) and is supposed to be valid during natural hypothermia. In hibernating marmots, for instance, we calculated a
Q10 value of 1.2 over a Tb range of 9.8°C
(Tb 7.8°C at
Ta 5°C vs.
Tb 17.6°C at
Ta 15°C).
This observation conflicts with those made by several investigators (8,
12, 21, 30, 35). They found an exponential relationship between
Tb and MR in the range where
Tb is not metabolically defended.
However, this is not the case in hibernating marmots. Metabolic heat
production can be better described as a function of the temperature
gradient between Tb and
Ta, which is valid for all data
obtained in deep hibernation and for those recorded at
Ta values 
5°C, i.e., above
the threshold of metabolic defense. We conclude that MR is actively
shut down and a Q10 effect may become irrelevant. As long as Tb
is close to Ta, minimum MR values can be reached irrespective of the actual
Tb, whereas
Q10 effects alone only allow two-
to threefold reduction of MR per 10°C decrease in
Tb.
Considering the effects of Q10,
one would expect that hibernators would reduce
Tb as fast as possible and force
the drop in Tb by behavioral and
physiological means, i.e., a stretched posture, sweating, and saliva
spreading or increased thermal conductance. Such a response has never
been reported for Alpine marmots or other species displaying
hibernation or torpor. On the contrary, marmots in the field huddle
together in extended family groups with close body contact in a
well-insulated hibernaculum. They show a curled body position and
synchronize their arousal events as well as the reentry into
hibernation (1, 3). Moreover, marmots additionally minimize their
thermal conductance to slow down cooling velocity and maintain this
level of reduced thermal conductance over the entire temperature range
where hibernation occurs. Our results indicate that thermal conductance
is nearly cut in half during hibernation compared with normothermia.
Such a significant reduction of thermal conductance attending the
entrance into torpor has previously only been found one time (31). The ability of an active reduction of thermal conductance during
hibernation is supposed to be of considerable energetic significance
but is not typical for hibernators (14) and should therefore be
interpreted with caution. In our study, thermal conductance has been
calculated in two different ways, and from single measurements of
normothermic marmots at very low
Ta (20 to 40°C)
we obtained values of 6-7 ml
O2 · kg1 · h1 · °C1.
These were directly calculated from
Tb,
Ta, and MR (data not shown) and
are within the range of thermal conductance of hibernating marmots. It
seems feasible that even normothermic marmots may reduce thermal
conductance down to the hibernation level, and thermal conductance
calculated from the regression slope possibly overestimates minimal
conductance in normothermia.
Nevertheless, marmots display a variety of adaptations, behavioral and physiological, which all together apparently prevent a rapid decrease of Tb. The uncoupling of metabolic heat production and absolute Tb during hibernation or torpor allows maintenance of very low MR even at high Tb as long as Tb is close to Ta. Alpine marmots experience temperatures that do not allow minimal metabolism over the whole hibernation season because Ta in natural hibernacula decreases exponentially from ~12-15°C in October to 0°C in spring (4). However, an active metabolic suppression would allow hibernation under optimal energetic conditions at least until mid-December. During December, Ta drops below the 5°C threshold, and energy requirements increase due to the active defense of Tb. Marmots are herbivorous and do not cache food but rely exclusively on their body fat reserves. Body fat is the only source to fuel both the 6-mo hibernation season and reproduction that occurs immediately after emergence from hibernation (3). However, winter is a major time of mortality in marmots (2), and unfavorable harsh winter conditions presumably have created selection for adaptations that reduce energy costs during hibernation. Reduced energy costs and lower body weight loss over winter enhance fertility and improve reproductive success in the following spring.
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ACKNOWLEDGEMENTS |
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We thank two anonymous reviewers for critical comments on the manuscript.
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FOOTNOTES |
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This study was supported financially by the Deutsche
Forschungsgemeinschaft, SFB 305 "Ökophysiologie
Verarbeitung von Umweltsignalen."
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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: S. Ortmann, Deutsches Institut für Ernährungsforschung, Arthur-Scheunert-Allee 114-116, D-14558 Bergholz-Rehbrücke, Germany (E-mail: ortmann{at}www.dife.de).
Received 8 March 1999; accepted in final form 5 October 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
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),
MRmin (
), and thermal
conductance (C; 
) of hibernating Alpine marmots as a function of
Ta. Solid line represents
Tb = Ta.
), and
summer-active (
) Alpine marmots. For regression analysis, values
below the thermoneutral zone, i.e., 
20°C
Ta in winter and