Cardiorespiratory and metabolic reactions during entrance into torpor in dormice, Glis glis
1 GSF National Research Center for Environment and Health, GMC
German Mouse Clinic Metabolic Screen, Ingolstaedter Landstrasse 1,
85764 Neuherberg, Germany
2 Department of Biology, Karl von Frisch Strasse, Philipps University
Marburg, 35043 Marburg, Germany
* Author for correspondence (e-mail: elvert{at}gsf.de)
Accepted 15 February 2005
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Summary |
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Key words: Glis glis, torpor entrance, metabolic depression, ventilation, heart rate
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Introduction |
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The edible dormouse (Glis glis) used in this study is known as a
true hibernator. They retreat into an underground burrow, their hibernaculum,
from October through March/April. However, they may also become torpid during
summer months. This may either be short daily torpor or extended periods of
estivation (Wilz, 1999). We
obtained long-term records of metabolic rate, heart rate, body temperature and
ventilation frequency in dormice spontaneously entering and arousing from
torpid states throughout the year. On average, each individual was recorded
for about five months, which allowed continuous observation of torpor episodes
at different ambient temperatures ranging from 028°C. The records
were used to analyse the sequence of physiological depression during
spontaneous entries into torpor. The timely relationship between heart rate,
ventilation, metabolic rate and body temperature may reveal whether all these
changes occur in parallel, or if they follow different time courses,
indicating a hierarchy of physiological inhibitions during entrance into
torpor. It will also answer the question whether metabolic rate, ventilation
and heart rate depression are a consequence of developing hypothermia or are
downregulated separately.
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Materials and methods |
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Body temperature and heart rate
Core body temperature (Tb) and heart rate
(fH) were recorded by a modified physiological
implantation system (Data Sciences, DSI, St Paul, USA). The
temperature-sensitive transmitter (model TA10ETA-F20; DSI, St Paul, USA) was
calibrated in a water bath within temperature ranges of 0.542°C
before implantation. Coefficients were calculated from the regression equation
(Elvert and Heldmaier, 2000a).
The dormice were anaesthetized with ketamine (60 mg kg1) and
xylacine (4 mg kg1). Anesthetics were injected i.p. The
transmitter for recording Tb, fH and
electrocardiogram (ECG) was implanted into the abdominal cavity and fixed with
sewing silk (1.5 metric) to the peritoneum. The electrodes of the transmitter
were sutured subcutaneously in the area of the right shoulder and the lower
left chest, corresponding to an Einthoven II recording (see
Kramer et al., 1993
).
Peritoneum and skin were sutured with resorbable catgut. Following the
operation the dormice were kept for recovery for 3 weeks at 1820°C
with food and water ad libitum. A magnetic switch allowed the
transmitter to be turned off to prolong battery life and records could be
obtained during repeated sessions for up to 2 years in individual dormice.
The receiver (RPC-1, DSI, St Paul, USA) was placed below the sleeping box (Fig. 1) and was connected to a consolidation matrix (DSI, St Paul, USA), which powered the receiver and transmitted the signals to an universal analog adapter (UA10, DSI, St Paul, USA). The adapter was calibrated by transmitter specific coefficients and controlled by a commercial computer software (Chart, DSI, St Paul, USA). The UA10-analog adapter and the computer control unit constitute the telemetry control unit (Fig. 1). For data analysis the signals were interfaced (interface 1: DACpad-71 B, Datalog, Moenchengladbach, Germany) and stored in 1 min interval on computer hard disk. The data acquisition was controlled by a self-developed software (QB45), which also included filter algorithms for suppression of noise and interference. The monitoring of the heart rate was done by scanning the signal input with a sampling rate of 1 kHz for 10 s. When several peaks were detected a mean value of peak interval was calculated. A continuous recording of ECG during entrance into torpor was enabled by splitting the analog output of the UA10-adapter and connecting an additional interface (UIM100A, model MP100, Biopac Systems, Santa Barbara, USA) with a sampling rate of up to 2 kHz. Data were stored on a further computer system.
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Metabolic rate
Oxygen consumption (metabolic rate,
O2) and carbon
dioxide production were recorded by pumping air through the nesting box with a
flow rate of about 35 l h1. The air was dried by cooling
traps (M&C Cooler, EPC, Ratingen, Germany). The flow rate was measured by
electronic flow rate meters (FM 360, Tylan, Eching, Germany). This
post-cuvette flow rate was corrected by the RQ to obtain a pre-cuvette flow
rate for calculation of metabolic rate. O2 and CO2
content was measured by an O2-analyzer (Ametek S 3a/II, Pittsburgh,
USA) and a CO2-analyzer (UNOR 6N Maihak, Hamburg, Germany). Both
analysers continuously compared the air from the nesting box with reference
air from the climate chamber and provided a resolution of 0.001% for
O2 and CO2. A magnetic valve system allowed switching to
a second reference channel every 55 min for automated zero readjustment and
calibration checks for 5 min.
O2 (ml
O2 h1) was calculated according to the equation
by Heldmaier and Steinlechner
(1981
).
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Ventilation frequency
Two different methods were used for monitoring the ventilation frequency
(fV). In a first set of experiments it was measured by
video recordings of ventilatory movements with an infrared camera on top of
the sleep and nesting box. This allowed measurements of ventilation in resting
dormice. In a second experimental design, the nesting box was replaced by a
total body plethysmograph to record ventilatory frequency even during
transitions, e.g. when entering torpor. The plethysmograph consisted of two
chambers with 810 ml of volume each
(Malan, 1973). The dormice
spontaneously entered one chamber, which was then used for measuring, and the
other one served as a reference chamber. Both chambers were closed when the
dormice settled quietly in the plethysmograph. A continuous and identical air
flow through both chambers supplied air to the dormice and allowed recording
of
O2 in
parallel. Second exits from both chambers were connected to a differential
pressure transducer (Halstrup EMA 48, Germany, range ± 50 Pa, accuracy
1%), which continuously compared the air pressure inside the chambers.
Pressure fluctuations caused by ventilation of the dormouse (temperature
changes of inspired and expired air) were continuously recorded and interfaced
by the data acquisition system described above (Biopac Systems, Santa Barbara,
USA). Body temperature, fH and ECG were simultaneously
recorded by the receiver directly placed below the plethysmograph. Ambient
temperature (Ta) was measured with a thermocouple placed
inside the sleeping box and the animal chamber of the plethysmograph,
respectively. Ventilation frequency was analysed in 5 min intervals with a
commercial software package (AcqKnowledge, Version 3.5.3, Biopac Systems).
From fV and oxygen consumption we calculated the oxygen
pulse to demonstrate the fast response and interaction of
fV and
O2.
Data analysis
We focussed our interest on monitoring the entrance into torpor at
different ambient temperatures. Wilz and Heldmaier
(2000) demonstrated in dormice
that the classification of dormancy into hibernation, estivation and daily
torpor due to seasonal responses is based on the same physiological mechanisms
for downregulation. Therefore, we concluded the recorded data as entrances
into torpor, regardless of duration of torpor bouts. The acquired data were
analysed using SigmaPlot 7.0. Statistical calculations were performed with
SigmaStat 2.01, Jandel Scientific. Mean values are reported ±
S.D. Data were tested for normality with Kolmogorov-Smirnov and
correlation coefficients were calculated following Spearman.
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Results |
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The ventilation pattern during resting phase I was always characterized by regular and quiet breathing movements (Fig. 4). This resting ventilation was about 40 breaths min1 at 28°C Ta. It increased in the cold to 114 breaths min1, as shown by the record in Fig. 3, top.
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Phase II pre-torpor adjustments
The resting phase was terminated by a sudden increase of
O2,
fH and fV
(Fig. 2). The mean duration of
this phase was 47 min. Ventilation rate rose to more than 260 breaths
min1 at 1.9°C Ta, which is about
five times the resting ventilation rate
(Fig. 3, top). The high
frequency included lower amplitudes of pressure changes and low volumes of
ventilation that closely resembles the ventilation pattern of panting. The
high frequency alternated with slower and regular breathing periods
(Fig. 4). Hyperventilation was
accompanied by a decrease in oxygen pulse, determined from oxygen consumption
and ventilation rate (sample recordings in Figs
2B and
5B). During the resting phase
the mean oxygen pulse was 54 µl O2 breath1 and
decreased to 27.4 µl O2 breath1 during
pre-torpor phase. Tb slightly rose to
36.97±0.91°C. The high ventilation rate was accompanied by a
significant increase in
O2 up to 80%
above resting
O2
to 1.99±0.59 ml O2 g1 h1
(Fig. 3, middle). Mean heart
rate increased significantly preceding entrance into torpor from 314.8 beats
min1 during resting to 372.3 beats min1
during pre-torpor phase (Figs
2,
3, bottom).
Phase III Reduction of physiological parameters
The period with high ventilation and
O2 was suddenly
terminated, and the dormice entered metabolic depression. In most cases this
starting point was marked by a peak in breathing frequency and
O2. Therefore,
the last metabolic peak was chosen as starting point of the reduction phase or
phase III. Since all parameters showed a nonlinear transient decline, which
did not allow a precise determination of the end point of transition, we
calculated the 90% decrease time instead, using RMR during the resting phase
as the initial value and
O2 during deep
torpor (see phase IV) as the final value. The duration of this decrease time
was determined for
O2,
fH, fV and Tb.
At all ambient temperatures the reduction of fV,
O2 and
fH occurred much faster than that of
Tb (transition time of fV versus
O2 versus
fH, n.s. (P>0.05). The reduction of
fV started with a steep decrease and dropped almost to the
level of resting ventilation within a few minutes. At 15°C
Ta the fV decreased from 200240
breaths min1 during pre-torpor phase to 4050 breaths
min1 during reduction phase
(Fig. 2). At 5°C
Ta fV was 300350 breaths
min1 during pre-torpor phase and decreased rapidly to
3040 breaths min1
(Fig. 5). The calculation of
the 90% decrease time, e.g. in this sample recording at 5°C
Ta revealed 82 min. It then decreased continuously until
the onset of intermittent ventilation (Fig.
4). The same pattern of steep reduction from high frequency into
torpor was observed at all other temperatures, too.
The slope of
O2 reduction
always paralleled that of fH (Figs
2,
5). At 5°C
Ta the decrease time of
O2 required 83
min and fH 93 min to perform 90% of the transition into
torpor. Comparable sample recordings of entrance into torpor at different
Ta show that the slope of reduction of
O2 for 5 and
15°C Ta is similar (Figs
2,
5). The oxygen pulse recovered
again during the beginning of the reduction period, but decreased later to a
mean value of 26 µl O2 breath1 at the end of
reduction phase. The slope of the decline of Tb increased
at low Ta and was most rapidly at the beginning of
entrance into torpor, indicating an exponential time course of
Tb. To compare the slopes of Tb
reduction the maximum cooling rate was determined between 3230°C
Tb and standardised as cooling rate per hour. At 5°C
Ta the cooling rate was at 8.5°C h1
and dropped at 28.2°C Ta to 1.1°C
h1. The 90% decrease time required was 343 min, which is
about three times the time required for metabolic, cardiac and ventilation
reduction.
Phase IV Steady state torpor
To obtain stable minimum values for physiological variables in deep
hibernation we used the final period of a torpor bout, i.e. 6020 min
prior to spontaneous arousal. Tb during steady state
torpor approached minimum values. Minimum
O2,
fH and Tb were determined as average
values over this period. Due to the small temperature gradient between expired
and ambient air it was impossible to determine ventilation during steady state
topor.
Metabolic rate was reduced to a fraction of that observed during the
resting phase (Fig. 2). Within
a temperature range of 714°C the mean value of
O2 was unchanged
at 0.0382±0.0037 ml O2 g1
h1, showing no relation with ambient temperature and, thus,
with body temperature (r2=0.097, P>0.05,
N=26). At Tb below 7°C the
O2 of individual
dormice increased again and they showed regulatory heat production preventing
a further decrease of Tb. The onset of this regulation
varied individually. The minimal
O2 observed was
0.0174 ml O2 g1 h1 at
Tb of 4.8°C for dormouse #R13G. At a
Tb of 14°C the minimal
O2 was 0.038 ml
O2 g1 h1 and increased to 0.25
ml O2 g1 h1 at 28°C
Tb (Fig.
6).
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Heart rate in steady state torpor was only a fraction of that observed
during resting (e.g. at 7°C Tb 8.2 beats
min1 instead of 314.8 beats min1 in the
awake but resting state). Below 7°C Tb the
fH accelerated corresponding to the elevated
O2 to defend
minimum Tb (Fig.
6). Above 7°C Tb the
fH in torpid dormice increased, depending on the
temperature up to 66 beats min1 at 31°C
Tb (Fig.
6).
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Discussion |
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Preparation for entrance into torpor
Immediately prior to metabolic depression dormice increased their
metabolism, ventilation and heart rate (phase II). This period of enhancement
lasted for about one hour, occurred regularly at each ambient temperature, and
may thus serve as a necessary preparation for the following depression of
metabolic rate. It was characterized by high ventilation frequency (up to 260
breaths min1), which increased from the resting level (phase
I) of about 64 to 114 breaths min1
(Fig. 3). The high frequency of
ventilation in combination with low pressure changes during ventilation
suggests that dormice showed a breathing pattern that closely resembled the
breathing pattern of panting. Withers already observed in pocket mice
(Perognathus longimembris) hyperventilatory phases that occured
during entry and arousal when exposed to Ta between
510°C, and a correlation of decreasing respiratory parameters with
the diminution of oxygen consumption
(Withers, 1977). Metabolic and
respiratory adjustments have also been observed for other hibernating mammals
(Malan et al., 1973
;
Landau and Dawe, 1958
;
Kristoffersson and Soivio,
1964
). Malan even noticed that the large increase of ventilation
that seemed to characterize the beginning of an arousal in marmots was not
accompanied by any significant increase of oxygen consumption that occurred
later in the arousal process. The continuously recorded data set of
ventilation frequency in dormice entering torpor indicates ventilation as an
instantaneous and most sensitive parameter for changes of physiological
states.
Metabolic and heart rate of dormice increased during the period of
enhancement in phase II by about 80% above the resting values
(Fig. 3) while body temperature
hardly showed a reaction. To illustrate the change of metabolic rate, heart
rate and body temperature mean values of phase I and phase II that preceded
entries into torpor were plotted against different Ta
values (Fig. 7). Metabolic and
heart rate of a sample dormouse increased with decreasing
Ta. An elevation from phase I to phase II could be
measured throughout the whole ambient temperature range. The oxygen pulse for
heart beat increased in parallel with metabolic rate to an elevated level
during phase II (Table 1).
Simultaneously, the oxygen pulse for ventilation in the pre-torpor phase, i.e.
the amount of oxygen consumed per breath was reduced by 50%, underlining the
suggestion of a panting like breathing pattern. This indicates an increased
heart metabolism that is maintained elevated during the reduction phase and in
deep torpor. These results confirm former studies on hibernating dormice or
woodchucks showing a significantly higher blood flow to the heart during
hibernation compared to other tissues or organs
(Wells, 1971;
Burlington et al., 1971
). A
more recent study performed on arousing Syrian hamsters (Mesocricetus
auratus) underlines this assumption
(Osborne and Hashimoto, 2003
).
The authors demonstrate that during arousal from hibernation large thermal
gradients exist within the body of the hamster that probably result from
coordinated, temporally specific restriction of blood to specific organs.
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Peaks in metabolic rate prior entrance into torpor have already been
observed in continuous recordings of pocket mice (Perognathus
longimembris, Withers,
1977), Djungarian hamster (Phodopus sungorus,
Heldmaier et al., 1999
) and
alpine marmots (Marmota marmota,
Ortmann and Heldmaier, 2000
).
Here we showed that this peak occurred in dormice during more than 140
investigated spontaneous entries into torpor and was always associated with an
increase in heart rate and ventilation frequency. The period of enhancement
(phase II) seems to be the terminating process for eumetabolism and
normothermia and simultaneously the preparatory step for an active, voluntary
depression into torpor. The necessity of this preparation remains an open
question, but it is possible that molecular or endocrinological mechanisms are
switched on or off to facilitate the physiological depression.
Ventilatory, metabolic and heart rate depression: key parameters for entrance into torpor
During phase III, the actual entrance into torpor, metabolic rate, heart
rate and ventilation are rapidly depressed. Almost instantaneously the dormice
terminated the high rates observed during phase II, returned to resting
levels, passed them and decreased their metabolic function in an exponential
manner towards torpor levels. The present findings in dormice revealed that
the decline of metabolism, heart rate and ventilation always occurred in
parallel and was independent from ambient or body temperature. A close
correlation between metabolic and heart rate has been confirmed in several
studies (Morhardt and Morhardt,
1971; Butler et al.,
1992
; Bevan et al.,
1994
; Boyd et al.,
1999
). Milsom et al.
(1999
) postulated that the
change in metabolic rate is mirrored by the change of heart rate and heart
stroke volume.
Body temperature of dormice decreased during entrance into hibernation.
Theoretically the decrease of body temperature could also be caused by an
increase in the rate of heat loss, i.e. thermal conductance as it was
suggested by Snyder and Nestler
(1990). Previous studies on
dormice revealed that the thermal conductance is not raised or reduced in
daily torpor, hibernation or estivation
(Wilz and Heldmaier, 2000
).
They calculated a mean minimum thermal conductance during entrance into torpor
of 0.056 ml O2 g1 h1
°C1, which is not different from the conductance of
normothermic dormice of the present study (C=0.063 ml O2
g1 h1 °C1). A
similar constancy of thermal conductance was also measured during entrance
into daily torpor in Djungarian hamsters
(Heldmaier and Ruf, 1992
).
This indicates that an increase in heat loss is not involved in the transition
into torpor. Instead thermal conductance is kept constant at a minimum level
causing a slow decline of body temperature. The decrease of
Tb lagged behind metabolic reduction and minimum body
temperature was reached about 6 h after metabolic functions had reached their
minimum. Ground squirrels (Citellus tridecemlineatus) similarly
decline breathing rate, heart rate and body temperature while the fall of
Tb lagged behind the drop of breathing and heart rates
(Landau and Dawe, 1958
). In
woodchucks (Marmota monax) entering hibernation spontaneously Lyman
(1982
) observed a simultaneous
decrease of heart rate with metabolic rate, and they also reached hibernation
values several hours before body temperature. In alpine marmots (Marmota
marmota) minimum
O2 is achieved
after 10 h, but body temperature virtually decreased throughout the entire
hibernation bout until the beginning of the next arousal
(Ortmann and Heldmaier, 2000
).
A similar relation between metabolism and body temperature was also observed
in Djungarian hamsters (Phodopus sungorus), indicating an active
suppression of metabolic rate, and the decline of body temperatures could be
interpreted as a consequence of the reduction of metabolic heat production
(Heldmaier and Ruf, 1992
;
Heldmaier et al., 1999
).
Present data obtained from dormice entering torpor support these results
they even complete the known results of active metabolic suppression
with a simultaneous depression of ventilation frequency and heart rate.
It has been suggested that the reduction of heart rate during entrance into
torpor is under parasympathetic control (see
Lyman, 1982), i.e. that heart
rate is modulated by changing the balance between parasympathetic and
sympathetic tone (Harris and Milsom,
1995
). Atropine increases heart rate by slowing the effects of the
parasympathetic nervous system while accelerating the effects of the
sympathetic nervous system. Treatment of hamsters with atropine during
entrance into hibernation elevates overall heart rate
(Lyman and O'Brien, 1963
;
Zosky, 2002
). Animals that
have been atropinized before they begin to enter hibernation rarely succeed in
entering hibernation. Lyman
(1982
) also observed in
marmots that arrhythmias in heart rate caused by skipped or extra beats as
occurred during reduction period disappeared with atropin treatment. Hence it
was concluded that the increased parasympathetic activity modulates and
decelerate heart rate (Lyman,
1982
; Zimmer et al.,
2000
). An inhibition of vagal activity led to an increase of heart
rate, even during apneic periods (Harris
and Milsom, 1995
; Zosky,
2002
), which eliminated the breathing coupled tachycardia as
described in dormice in Fig. 4
(Kristofferson and Soivio, 1964;
Tähti and Soivio, 1975
;
Steffen and Riedesel, 1982
;
Grigg and Beard, 1996
).
In Spermophilus lateralis it was shown that simultaneously to the
decelerated heart rate the electrocardiogram was prolonged during deep
hibernation (Steffen and Riedesel,
1982). At Ta=7°C they measured a duration
from P to T wave of 0.062±0.09 s. A detailed analysis of ECG pattern
revealed that dormice also develop arrhythmias during entrance into torpor and
a prolonged ECG duration (Figs
8 and
9). At
Tb=2.2°C the PT-duration lasted more than one second
(Fig. 9A) while during
normothermia it was maintained constant at 0.065±0.0067s over a wide
range of Ta (Fig.
9B). The occurance of extra systoles and the prolongation of the
ECG signal supports the assumption that the decrease in heart rate in dormice
is also under control of parasympathetic tone. This suggests that
parasympathetic activation and the initial changes in heart rate may be
generally necessary for entrance into a torpid state
(Milsom et al., 1999
;
Zimmer et al., 2000
). Milsom
and colleagues (1993
) showed
that stimulation of the vagus nerve reduced the mean heart rate by about 80%
in normothermic as well as in hibernating squirrels (Spermophilus
lateralis). Parasympathetic tone was also involved in homeostatic
regulation during deep hibernation (Harris
and Milsom, 1995
), but it was emphasized that the reduction in
body temperature associated with hibernation did not block vagal
conduction.
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|
Data of the present study support a paradigm that entrance into torpor is
characterized by a controlled reduction of metabolic, cardiac and ventilatory
activity. Several studies suggested that hypercapnia and hypoxia may induce or
facilitate entry into torpor by suppressing metabolism
(Studier and Baca, 1968;
Williams and Rausch, 1973
;
Schäfer and Wünnenberg,
1976
; Kuhnen et al.,
1983
). But there are also contrary observations described in the
literature. Withers noticed that the pocket mouse exposed to
Tas of 510°C spontaneously entered torpor even
with ad libitum food. But no facilitation of entry was observed
breathing 6% CO2 (Withers,
1977
). He assumed that hypercapnia and hypoxia are unlikely to be
considered as important factors for the initiation of torpor, but this was not
apparent for P. longimembris. The present study on dormice focussed
on natural and undisturbed entries into torpor. Although we never exposed them
to hypercapnic or hypoxic conditions they easily enter torpidity when being
food reduced within a temperature range of 028°C
Ta. However, we observed fluctuations in the RQ during
entries into torpor within 07°C Ta
(Elvert and Heldmaier, 2000b
).
But these fluctuations were not caused by hypercapnia or hypoxia. The decrease
of RQ closely paralleled the decrease of Tb in phase III.
During normothermia and under food restriction the RQ was about 0.7 indicating
a preferential combustion of lipids and was not related to hyperventilation or
increased metabolic or heart rate during phase II. Bickler
(1984
) and Malan
(1988
) observed that the
entrance into daily torpor or hibernation is accompanied by a falling
respiratory exchange rate und suggested that this contributes to a
CO2 retention. Drops of RQ at the beginning of entry into torpor
have been observed for several other species
(Snapp and Heller, 1981
;
Bickler, 1984
;
Malan, 1986
;
Nestler, 1990
). Hence,
inhibitory effects of CO2 retention and respiratory acidosis on
thermoregulatory structures, glycolysis, neural activity and brown fat
thermogenesis have been discussed (Malan
et al., 1973
). But there is still no evidence that indicates
carbon dioxide retention generally acts as a stimulating factor for entrance
into hibernation under normoxic conditions. There may be an accumulation of
carbon dioxide in body fluids during entrance into torpor at very low ambient
temperatures, as was described for dormice
(Kreienbühl et al., 1976
;
Elvert and Heldmaier, 2000b
).
Blood analyses have shown that when the temperature of the blood decreased,
its pH increased and PCO2 decreased
(Musacchia and Volkert, 1971
;
Kreienbühl et al., 1976
;
Rodeau and Malan, 1979
;
Malan, 1982
). To maintain a
constant PCO2 and pH, additional storage of
large quantities of CO2 are required
(Malan, 1982
). Hence, it seems
that CO2 retention contributes to the control of a constant pH at
low temperatures as it was discussed for dormice
(Elvert and Heldmaier, 2000b
).
This further indicates a relative respiratory acidosis
(Bharma and Milsom, 1993
). It
is thus unlikely for hypercapnia or hypoxyia to be the cause of metabolic
depression but possibly facilitates a continuous decrease into deep
hibernation.
The present data suggest that the transition into torpor is initiated by an endogenously programmed and interacting pattern of physiological inhibition, with actively downregulated ventilation, metabolic rate and heart rate to the low level in torpor. This study demonstrates that the entrance into torpor is a complex, but well coordinated interacting system, showing shifts in neurological control and changes in acid-base balance. But a detailed endocrine or neural signalling of overall depression as well as the function of the preparatory phase of hyperventilation and increased activity is not known. A clarification of mechanisms initiating the entrance into torpor might be possible when focussing on the preparatory phase.
Abbreviations
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Acknowledgments |
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References |
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