Telemetric investigation of hibernation and post hibernal normothermy of European hamsters kept under semi-natural conditions
Waßmer T.1 and Wollnik F.2
1 Lehrstuhl Verhaltensbiologie, Fakultät für Biologie, Universität
Konstanz, Postfach 5560 M618, D-78434 Konstanz, Germany
2 Abteilung Tierphysiologie, Biologisches Institut, Universität Stuttgart,
Postfach 80 11 40, D-70511 Stuttgart, Germany
Keywords
Cricetus cricetus, body temperature, locomotor activity, above ground
activity, torpor, immergence, emergence, hibernation pattern, circadian
cycle, oestrous cycle
Introduction
European or common hamsters belong to the rodent family Cricetidae
and are closely related to the more popular Syrian or golden hamsters.
The European hamster is widely distributed in the temperate Western Palaearctis
between 44 and 59 °N and 5 - 95 °E. In Central Europe its range
reaches the western border with disjuncted local occurrences in France
(Strasbourg), the Netherlands and Germany. Until most recently, the European
hamster was feared as a pest animal in agriculture. During the last decades,
however, there was a serious decline in the population numbers of the European
hamster, which forced the German authorities to place the old pest animal
on the red list of threatened species. European hamsters are solitary living
medium sized (200 - 500 g) food generalists living in burrows. They reproduce
2 - 4 times a year with a mean litter size of 6 and reach an age of 3 -
4 years (Niethammer 1982).
During wintertime, all homeothermic animals living in cold and temperate
latitudes as well as in continental climates need more energy to keep their
body temperature (Tb) around 38 °C. In addition to low ambient temperature
(Ta), food shortage further increases the need for energy conservation.
Depending on body size, there are various strategies to reduce energy loss.
Big animals can reduce energy expenditure to 50 % by growing thick winter
fur whereas small mammals can use this strategy only to a certain degree
because of their relatively large body surface (Heldmaier 1990). Reduction
of body mass prior to winter and episodical or periodical reduction of
Tb are very effective strategies to reduce total energy expenditure during
the hibernation season, e.g. to 77 % of basal in the golden hamster (McKee
and Andrews 1992).
Like many animals of seasonal changing habitats, the European hamster
shows seasonal rhythms in body mass, reproduction and the control of Tb.
Many experiments conducted under constant ambient conditions proved this
rhythmicity to be at least partially endogenous: seasonal rhythms continue
even in the absence of external triggers. In nature, this endogenous seasonality
is synchronised to the external seasons by time cues like photoperiod and
Ta (Masson-Pévet et al. 1994).
Thermo-sensitive telemetry is a rather suitable method for continuous
recordings of Tb in undisturbed animals. This paper describes an experimental
set-up in semi-natural conditions and presents preliminary results on the
time course of Tb during hibernation and during the normothermic period
immediately after termination of heterothermy. In addition, our experimental
set-up allowed recordings of the frequency and duration of times during
which the animals left their hibernacula and were located above the ground
(above ground activity, AGA). A third variable recorded was overall locomotor
activity (LA).
Materials and Methods
The thermo-sensitive HF-transmitters used were developed by the
Technical Workshop of the University of Konstanz. They were of cylindrical
shape with maximum dimensions of 1.8 (diameter) by 4.2 cm (height) and
a maximum weight of 18.6 g, corresponding to approximately 5 % of the body
weight of a medium sized European hamster. Dimensions and weight were mainly
due to the relatively large batteries producing a 3 Volt output for 950
mAh. Transmitters were encoated into a mixture of bees wax and paraffin
suitable for implantation into the abdominal cavity of the hamsters.
In each of two winters (1994/95 and 1995/96), 12 European hamsters
(6 females and 6 males) were individually housed in wire mesh cages of
0.8 m (length) by 0.8 m (width) by 1.1 m (height). Cages were buried 0.6
m into the ground of an outdoor enclosure near the university campus and
filled with soil in order to allow the animals to dig their own burrow
inside the cage. Each cage was equipped with two spiral shaped antenna
fixed into the PVC platforms at the bottom and the top of the cage.
All transmitters used the same carrier frequency of 14 MHz. They
were screened off each other by the metal cages in case of the 12 implanted
transmitters and by a small faraday cage built around the reference transmitter
(#13) used for the measurement of Ta at ground level (Fig. 1). Transmitter
#14 was buried in the soil at about the same depth as the bottom of the
cages and was used as a reference for soil temperature. Inside each cage,
the signals of the transmitter could be received either by the top or by
the bottom antenna. In order to achieve simultaneous recordings and to
minimise the distance between transmitter and receiver, every transmitter
had its own single-super-heterodyne receiver placed on top of the cage.
Temperature encoding pulse frequencies were converted into digital signals
and passed on as opto-coupled signals. For the measurement of locomotor
activity, field strengths of pulses were passed on as analogue opto-coupled
signals. The recording interval and sensitivity of the receivers were controlled
by an IBM compatible personal computer (PC) containing a microcontroller
card and running on a special developed MS-DOS-program that processed and
stored the data. When the recording was interrupted for a specified time,
a switch of the antenna was triggered by the microcontroller. Temperatures
of all 14 transmitters were simultaneously measured as moving averages
on 32 pulse frequencies within the recording interval (usually set to 5
min). In order to eliminate recording artefacts, the moving average procedure
required 6 pulse frequencies with a specifiable amount of constancy (maximum
deviation usually set to be less than 0.5 %). AGA was recorded as the percentage
of an interval, during which signals were received by the top antenna.
In addition, differences between the field strength of consecutive pulses
were used to compute LA in a second moving average procedure. Incoming
data could be viewed on the PC screen and were stored on the hard disk
of the PC as well as on a floppy disk.
Periodicities of biological rhythms such as daily cycles as well
as oestrous cycles were verified using the Chi2-periodogram (Sokolove and
Bushell 1978).
Results
Due to technical problems and natural mortality, only a total of
13 complete and 5 partial hibernation patterns (HPs) was recorded. Figure
2 shows a complete recording of the HP of a female hamster. As in all hibernating
species studied so far, hibernation of the European hamster is organised
in discrete "bouts" of hypothermia (hibernation bouts, HBs),
separated from each other by inter-bout normothermy (IBN). Twelve hamsters
showed a regular pattern of 7 - 44 deep HBs with a decline of Tb near to
soil temperature (minimum Tb = 0.97 °C) and durations > 24 h (maximum
bout length = 165.2 h). Three other animals showed only a few deep HBs
that were mixed with shallow HBs of shorter duration and separated by rather
long periods of IBN. Finally, 3 hamsters did not hibernate: they showed
no HBs at all. Hibernation started between October 2 and January 8 and
ended between January 29 and April 9. Most hamsters stayed in their burrow
for 4 - 39 days before the first decline of Tb below 30 °C and remained
inside their burrow for 0.5 - 22 days after the final rewarming in spring.
However, 7 out of 13 hamsters interrupted hibernation for brief periods
of times and appeared above ground. These animals spent a total of 0.43
- 401.74 h above ground. In animals showing a regular pattern of HBs with
only short periods of IBN (Fig. 2), hibernal AGA was absent, whereas short
episodes of AGA occurred in animals showing dispersed HPs within extended
times of IBN. Even in those hamsters that did not show any HB, AGA was
considerably reduced as compared to normothermic times. These animals stayed
in their burrows for periods of up to 4 weeks without any AGA.
Of the total duration of the hibernation season about 1.6 - 80.2 % were
spent in hypothermia (Tb below 30 °C) and 19.8 - 98.4 % in IBN. Mean
Tb during hibernation ranged between 13.46 and 37.47 °C. LA was reduced
to 15 % compared to the normothermic conditions before and after hibernation.
The longest HBs were observed between end of December and end of March.
Each HB could be subdivided into a period of cooling-down (entry),
a plateau phase with Tb levels around Ta, and a warming-up interval (arousal)
(Fig. 3). During entry into hypothermia, Tb decreased quite slowly indicating
a passive cooling along the temperature gradient. However, the occurrence
of temporary rewarmings accompanied by peaks in LA indicate a regulated
rather than a purely passive process. In the beginning of arousals from
hypothermia, Tb increased first slowly to about 10 °C and then rather
rapid until reaching normothermic Tb. The explosive increase in Tb was
accompanied by the first occurrence of LA indicating the begin of thermogenesis
through shivering of the animal. During the plateau phase of the HB, every
extreme change in ambient temperature was followed by a similar change
of Tb. As a result, Tb fluctuated within a range of 10 °C without leading
to an interruption of the typical time course of a HB (Fig. 3). Time-lagged
correlations between Ta and Tb were a rather common phenomenon observed
within the plateau phase of HBs. Nevertheless, some hamsters showed spontaneous
fluctuations in Tb during the plateau phase that were not caused by Ta.
These low amplitude oscillations (less than 3 °C) showed a considerable
regularity, increased in amplitude and finally lead to termination of the
HB during the rising phase of the last oscillation.
During posthibernal normothermy, a 24h-rhythm was clearly visible
in Tb, AGA and LA (Fig. 4). In addition to daily cycles, the recordings
also allowed detection of the oestrous cycle in female hamsters. During
the posthibernal time from spring until summer 1996, a four-day rhythmicity
in the daily maximum of Tb was observed in 3 out of 5 female European hamsters.
Identification of the oestrous cycle in females was also possible by the
analysis of mean daily percentage of AGA in 2 out of 5 animals and within
a single female by analysing the daily sum of LA. It has to be evaluated
whether the analysis of the oestrus cycle can be used to determine the
onset and offset of the reproductive period during long-term recordings.
Discussion
Telemetric measurements of Tb in undisturbed animals over the entire
hibernation season are fundamental to investigate the temporal organisation
of hibernation and its relationship to environmental variables. The present
study introduces first results on the time course of Tb during a long-term
registration of hibernation in European hamsters kept under semi-natural
conditions. The recordings demonstrated a variety of individual differences
in the pattern of heterothermy confirming previous studies under laboratory
(Waßmer & Wollnik 1996) as well as semi-natural conditions (Wollnik
and Schmidt 1995). The finding that some animals showed only dispersed
HPs or no torpor at all proved that this is clearly not an artefact occurring
only in laboratory conditions. However, the exact nature of this behaviour
remains unclear. On one hand, it may be that the failure to hibernate indicates
some sort of constrain either because of unsuitable external conditions
or because of some physiological problem of the animal. On the other hand,
it may be that there is a genetically fixed percentage of animals not entering
deep hibernation in a facultative hibernator as the European hamster and
these animals may have some advantage at least during not so harsh winters.
The present study revealed a number of interesting features of the
HP of European hamsters. For example, due to the special set-up of the
two antennas, additional information was obtained on the general activity
of the animals as well as their appearance above ground. As far as we know,
this is the first study of hibernating animals with simultaneous measurements
of Tb and above ground activity. These measurements demonstrated that some
animals leave their burrow during IBN. However, AGA is a rather rare event
observed only in those animals with dispersed HPs or no torpor at all.
Information on AGA could also be used to verify the hypothesis that males
end their hibernation period earlier than females, but remain in their
burrows in order to develop their testes before emergence in spring (Michener
1992). The data available so far for the European hamster did not reveal
any sex-related difference in the timing or amount of hypothermia.
Furthermore, the present study revealed interesting information
on the time course of Tb during hypothermia. For example, the decrease
of Tb during entry into hypothermia was occasionally interrupted by a brief
increase of Tb and accompanied activity suggesting a regulatory increase
in the metabolic rate in order to slow down the cooling process (e.g. Fig.
3). Similar results were found in a laboratory study investigating the
effects of experimental cooling in active European hamsters. Tb often dropped
in a stepwise manner indicating a similar stepwise decrease of the homeostatic
setpoint (Malisch et al. 1975). Furthermore, in a previous laboratory study
on European hamsters, we observed a stepwise decrease of Tb from the daily
minimum of normothermic Tb to short and shallow HBs and finally to deep
HBs in the beginning of the hibernation season indicating a gradual change
of the thermoregulatory set point (Waßmer and Wollnik 1996). During
the plateau phase of HBs, Tb was closely correlated with Ta (Fig. 3). However,
Tb remained constant or increased when Ta decreased below a certain critical
value. The present results thus confirm previous studies demonstrating
that thermoregulation is not arrested during deep hypothermia (Heller and
Collivier 1974, Heller et al. 1977). In contrast to the rather common phenomenon
of a time-lagged correlation between Ta and Tb during deep hibernation,
some animals showed spontaneous low amplitude oscillations in Tb that were
not caused by changes in Ta. Arousal from such HBs occurred during the
rising phase of the final oscillation. A phenomenon like this was recently
reported from a laboratory study on ground squirrels kept under constant
darkness and temperature (Grahn et al. 1994) and was interpreted as an
indicator of endogenous control on bout duration. The time-course of arousals
from HBs could be separated into a slow rewarming up to approximately 10
°C, followed by an extreme warming rate that was accompanied by increasing
LA (Fig. 3). These findings support the view, that initial heat production
is generated through nonshivering processes of uncoupled respiration in
brown fat mitochondria, followed by shivering thermogenesis of involuntary
tonic or rhythmic contractions of muscles (ATP-hydrolysis) (Heldmaier et
al. 1989).
Finally, the present recordings demonstrated not only daily rhythms
in Tb, AGA and LA during posthibernal normothermy, but also oestrous correlated
changes in the daily maximum of Tb and mean daily AGA rather similar to
oestrous correlated changes of Tb previously reported for golden hamsters
(Refinetti and Menaker 1992), marsupials (Rose and Jones 1996) and rats
(Kent et al. 1991). The rather high levels of AGA, reflected also in Tb,
are caused by the high level of oestrogen during the night of oestrous
(Takahashi and Menaker 1980) and will most likely increase the chances
of encounter with a potential mate.
In conclusion, the experimental set-up of our study revealed a number
of fascinating aspects on the ecology and physiology of hibernation in
the European hamster under semi-natural conditions. Supported by the DFG
(Wo 354/2).
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