comparison of surface temperature in 13-lined ground squirrel (spermophilus tridecimlineatus) and...
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Comparative Biochemistry and Physiol
Comparison of surface temperature in 13-lined ground squirrel
(Spermophilus tridecimlineatus) and yellow-bellied marmot
(Marmota flaviventris) during arousal from hibernation
P.K. Phillips*, J.E. Heath
Department of Molecular and Integrative Physiology, University of Illinois, Urbana, Illinois, USA
Received 12 March 2004; received in revised form 3 June 2004; accepted 6 June 2004
Abstract
Surface temperatures (Ts) of eight 13-lined ground squirrels and seven yellow-bellied marmots were measured during arousal from
hibernation using infrared thermography (IRT) and recorded on videotape. Animals aroused normally in 5 8C cold rooms. Body temperatures
were recorded during arousal using both cheek pouch and interscapular temperature probes. Warming rate in arousal was exponential. Mean
mass specific warming rates show the squirrels warm faster (69.76 8C/h/kg) than the marmots (4.49 8C/h/kg). Surface temperatures (Ts) for
11 regions were measured every few minutes during arousal. The smaller ground squirrel shows the ability to perfuse distal regions without
compromising rise in deep body temperature (Tb). All squirrel Ts’s remained low as Tb rose to 18 8C, at which point, eyes opened, squirrels
became more active and all Ts’s rose parallel to Tb. Marmot Ts remained low as Tb rose initially. Each marmot showed a plateau phase where
Tb remained constant (mean Tb 20.3F1.0 8C, duration 9.4F4.1 min) during which time all Ts’s rose, and then remained relatively constant as
Tb again began to rise. An anterior to posterior Ts gradient was evident in the ground squirrel, both body and feet. This gradient was only
evident in the feet of the marmots.
D 2004 Elsevier Inc. All rights reserved.
Keywords: Arousal; Hibernation; Ground squirrel; Infrared thermography; Marmot; Surface temperature; Vasomotion
1. Introduction
The adaptive advantage gained by the use of hibernation
is considerable. Richardson’s ground squirrel (Spermophilus
richardsonii) can save 88.8% of its total energy over a
season by using hibernation (Wang, 1978). The periodic
arousals that are required, however, are also quite energy
expensive. That same Richardson’s ground squirrel spends
83.4% of its total energy during hibernation season on
arousal (Wang, 1978).
In arousal, heat production continues to increase by what
appears to be a positive feedback mechanism (Hammel,
1095-6433/$ - see front matter D 2004 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpb.2004.06.005
* Corresponding author. Current address: Department of Biological
Sciences, Florida International University, University Park OE 167, 11200
SW 8th St., Miami, Florida 33199, USA. Tel.: +1 305 348 6163; fax: +1
305 348 1986.
E-mail address: [email protected] (P.K. Phillips).
1986). Rate of warming varies not only between species and
individuals, but also within the same animal (Lyman and
O’Brien, 1986). This variation occurs based on size differ-
ences as well as the time in the hibernation cycle when the
animal is aroused. Size of the animal appears to play a large
role in rewarming capabilities (Geiser and Baudinette,
1990). The big brown bat (Eptesicus fuscus), which relies
heavily on brown adipose tissue (BAT), arouses in one-
quarter the time it takes the larger golden-mantled ground
squirrel (Spermophilus lateralis), which is less dependent
on BAT, to arouse (Hayward et al., 1965).
Differential vasomotor control refers to more tightly
regulated vascular changes in specific surface areas that
could lead to changes in heat loss. By selectively dilating
vessels to certain areas, heat exchange is increased in that
location while vessels in other regions can remain con-
stricted to minimize heat loss. Although small rodents can
set the hypothalamic thermostat to a very low level, there is
ogy, Part A 138 (2004) 451–457
P.K. Phillips, J.E. Heath / Comparative Biochemistry and Physiology, Part A 138 (2004) 451–457452
no evidence for differential vasomotor control and the
corresponding body temperature (Tb) differential (warmer
anterior regions compared to posterior) in very small (b100
g) animals. This includes mice (Peromyscus leucopus),
Mongolian gerbils (Meriones unguiculatus) which remain
euthermic, and the marsupial planigale (Hudson, 1967; Klir
et al., 1988; Dawson and Wolfers, 1978). The species
involved in this study are much larger, however, and this
temperature differential should be apparent.
In euthermic 13-lined ground squirrels (Spermophilus
tridecimlineatus), any vasoconstriction results in a marked
difference in the temperature of various body parts (Lyman
and O’Brien, 1960, 1963). Vasomotor adjustments are also
common in euthermic golden hamsters (Mesocricetus
auratus) (Pohl, 1965). Early studies on these two species
found only one sixth of the body warmed during early
arousal, which corresponds to thoracic volume (Mokrash et
al., 1960). Slow posterior warming during arousal seems to
indicate high posterior peripheral resistance and sluggish
flow front to back with unrestricted flow in later arousal to
warm the posterior (Lyman and O’Brien, 1960, 1963). In
yellow-bellied marmots (Marmota flaviventris), the lag of
rectal temperature indicates vascular rerouting which occurs
when shivering begins at which point there is a remixing of
blood from the warm anterior region to the cold posterior
(Smith and Hock, 1963). There is a decrease in blood
pressure and accompanying decrease in peripheral resist-
ance as rectal temperature rises, indicating dilation of
previously constricted areas (Lyman, 1982).
In 1967, Johansson suggested the differential vaso-
constriction in arousal could be followed using infrared
thermography (IRT). That same year, Hayward and Lyman
(1967) used IRT on a shaved bat to show areas around
brown adipose tissue are the first to warm. To this point,
however, IRT has not been used to look at arousing animals,
and changes in temperature during arousal have not been
studied or considered for many years. Recently, IRT has
been used to evaluate surface temperature (Ts) changes in
golden-mantled ground squirrels (S. lateralis) subjected to
hypoxia (Tattersall and Milsom, 2003), although no
distinction was made between anterior or posterior regions
for the flanks or feet. We used IRT to measure Ts in
euthermic woodchucks (Marmota monax) (Phillips and
Heath, 2001).
In 1995, we showed that the ability to regulate surface
temperature scales with size (Phillips and Heath, 1995)
larger animals being better able to regulate Ts primarily
because of the smaller surface area to volume ratio. Here,
we used IRT to study two species of different size during
arousal from hibernation not only to see if the vasomotor
changes can be detected but also what sort of different
responses can be detected between species which differ in
size by one order of magnitude. We expect to be able to
detect changes in surface temperature as the animals warm,
that the anterior regions will warm more rapidly (differential
vasoconstriction) and Ts of those regions will be maintained
at the higher temperatures. In addition, we expect that the
smaller species (squirrel) will show limited ability to
regulate Ts of specific regions when compared to the larger
marmot.
2. Materials and methods
All animals were being housed in cold rooms being
maintained in constant darkness at 5 8C. The squirrels had
been trapped in November in Illinois, and were housed at
the University of Illinois. Since ground squirrels eat during
the hibernation season, they were provided with food and
water at all times. They were placed in individual cages
with wood shavings for bedding and covered with large
plastic bags to prevent drafts from reaching the animals.
The marmots were trapped in summer in Colorado and
housed at Temple University. Because marmots cease
eating during the hibernation season, food was removed
from the cages in October but water was available at all
times, as was cotton bedding. Approval was granted
through appropriate channels at each study site prior to
beginning any studies.
Eight 13-lined ground squirrels and seven yellow-bellied
marmots were observed during arousal from hibernation
using an Inframetrics model 525 infrared imaging system
that has been described in detail previously (Mohler and
Heath, 1988; Klir et al., 1988; Klir and Heath, 1992; Phillips
and Heath, 1992). In the ranges being used, 10 and 20 8C,the system has a sensitivity of +0.04 and 0.08 8C,respectively. Squirrel studies were conducted during Febru-
ary 1990, December 1990, and February 1991. Marmot
studies occurred in February and early March 1991.Ambient
temperature (Ta), body temperatures (Tb) and temperature of
a constant object within the field of view were measured
with a Physitemp BAT-12 digital thermometer
(sensitivityF0.1 8C) and a copper constant thermocouple.
Images produced by the Inframetrics systems during each
arousal period were saved on standard VHS videotape for
later analysis.
Body temperatures were measured at all times during
arousal. Two methods for measuring Tb were employed.
Since check pouch temperature has been shown to parallel
brain temperature in hibernators (Lyman and Chatfield,
1950), a thermocouple was placed into the cheek pouch of
each animal while in deep hibernation. Additionally, five
squirrels and all marmots had an interscapular thermocouple
re-entrant tube inserted just prior to filming, similar to the
techniques used in other studies (Florant et al., 1978; Florant
and Heller, 1977; Heller and Hammel, 1972). The area was
cleaned with a betadine solution and a small incision was
made in the skin between the scapulae of the hibernating
animal. A 5-cm length of sterile plastic tubing just large
enough to permit insertion of a 35-gauge thermocouple wire
was inserted subcutaneously and posteriorly to a length of 4
cm in the marmots, 3 cm in the squirrels and secured with
Fig. 1. Line drawing of a ground squirrel indicating the regions into which
IR images were divided for analysis and measurement. Images of marmots
were divided in the same manner: (1) ear, (2) eye, (3) nose, (4) head, (5)
front foot, (6) rear foot, (7) front flank, (8) rear flank, (9) back, (10)
abdomen, (11) tail.
P.K. Phillips, J.E. Heath / Comparative Biochemistry and Physiology, Part A 138 (2004) 451–457 453
tape. The thermocouple was inserted into the tube and also
secured with tape. Because of the potential danger of using
general anesthesia or sedatives in hibernating animals,
minimal local anesthesia (32 mg/kg ketamine) was admin-
istered subcutaneously prior to the initial incision. Anti-
biotic ointment containing sulphur was applied to the area
after insertion and at the end of the session when the tube
was removed. Because interscapular temperature followed
cheek pouch temperature very closely and the animal was
less likely to remove this thermocouple during arousal,
interscapular temperature was the preferred means of Tb
measurement.
In each case, handling of the animal to begin Tb
recording was sufficient to induce arousal. Because there
is a direct relationship between torpor length, Tb and Ta(Hudson, 1967), all animals were allowed to arouse in the
rooms in which they were housed, which were maintained at
5F1 8C. Squirrels were set on a shelf in the cold room to
arouse. This eliminated the need to remove the pixels that
corresponded to the cage wires during analysis of the tapes.
Marmots were returned to their individual cages, but with
bedding removed (replaced upon completion of the trial).
The entire arousal period was recorded. No specific Tb
was selected to signify the end of the trial. Rather, when Tsof the various regions achieved that for euthermic animals at
Ta of 5 8C, the session was ended. Occasionally, in the case
of the squirrels, activity level of the animal precluded an
ability to continue filming. Tb was measured periodically
(every 3–5 min) and this time was noted on the tape by a
series of isothermal measurements. Surface temperatures
(Ts) were measured at each of these times during analysis of
the tapes. Eleven regions were distinguished in the measur-
Table 1
Mean Ts+S.D. (8C) at selected interscapular temperatures during arousal: ground
Tisc Ear Eye Nose Head F. foot R.
7 7.5F1.0 6.8F0.7 7.3F0.8 7.1F0.9 7.1F0.9 6.7
15 11.0F1.5 10.0F1.4 7.2F1.0 9.0F1.1 7.1F1.3 6.3
24 17.5F2.5 14.8F1.9 9.2F1.6 12.6F1.3 9.5F0.9 7.6
32 22.3F2.0 20.7F2.6 13.0F2.7 15.7F2.2 11.3F1.9 8.1
ing of Ts (Fig. 1): eye, ear, nose, head (not including the
previous), front flank, rear flank, abdomen, back, front foot,
rear foot, and tail. Because of the curled-up posture of the
animal, it was generally not possible to see all four feet and
often the tail was not visible.
3. Results
Statistical analysis, such as mean Ts or warming rate at
various times during arousal is not possible due to the
variance in arousal times for the 15 subjects. Tables 1 and 2
show mean Ts for each area at selected times during arousal
based on Tb. Graphing the temperature changes over time
gives a better indication of what was occurring, however.
Examples of the data obtained via the analysis of the tapes
are shown in Figs. 2–7 for one squirrel and one marmot.
The observed sequence of events and analyzed data were
similar for all trials of each single species. Space limitations
prevent illustrating the data for all eight squirrels or seven
marmots.
Average Tb at the beginning of arousal for the squirrels
was 7.7F2.1 8C (range 6.0–12.3 8C). The squirrels requiredan average time of 1.63F0.37 h to arouse (range 1.4–2.1 h).
Mean mass of the eight animals was 225F12 g. Mass
specific warming rate for the squirrels was 69.74F19.26 8C/h/kg. Figs. 2–4 show the data for a 200 g female in which
interscapular temperature was measured. The warming
curve of interscapular temperature versus time can be fitted
to an exponential function (R2=0.937). This was also the
case for all other squirrels, although the exponential fit was
not always significant. This is likely due to the difficulty in
measuring Tb via cheek pouch for the entire session, since
some squirrels did not have re-entrant tubes inserted.
Squirrels all had a tendency to remove the cheek thermo-
couple at about the same point as they opened their eyes.
All squirrels began to shiver visibly as Tb reached
12–13 8C. The point at which the eyes opened was noted
visually and is easily detected on the IR tapes. When eyelids
are open, the eyeball bglowsQ in IR, demonstrating the
higher Ts of the eyeball versus the eyelid. This occurred at
Tb of 18.7F1.05 8C and squirrels became quite active.
Visible shivering had generally ceased in each subject when
Tb reached 21 8C. Ts’s attained at the end of each trial were
comparable to those maintained by a euthermic ground
squirrel at Ta of 4 8C (Phillips, 1992; Phillips and Heath,
1995).
squirrels
foot F. flank R. flank Back Abdomen Tail
F0.7 7.3F0.6 7.0F0.6 7.1F0.5 7.0F0.6 6.6F0.5
F1.0 8.7F1.4 6.7F1.0 8.1F1.2 7.2F1.2 6.0F0.8
F0.7 12.0F1.2 7.8F1.1 11.1F1.5 9.0F0.7 6.6F0.9
F0.9 13.7F2.2 10.1F2.3 13.4F1.8 10.3F1.3 8.2F3.7
Table 2
Mean Ts+S.D. (8C) at selected interscapular temperatures during arousal: marmots
Tisc Ear Eye Nose Head F. foot R. foot F. flank R. flank Back Abdomen Tail
11 7.6F1.1 7.7F0.7 6.1F0.8 6.8F0.5 6.7F1.6 6.8F1.3 6.8F0.8 6.6F1.0 6.8F0.8 6.8F0.8 6.2F1.3
18 11.4F1.7 11.5F1.2 6.1F0.6 8.7F1.2 6.0F1.1 5.7F0.9 6.5F1.0 5.4F1.1 5.8F1.2 5.9F0.8 4.7F0.6
25 17.2F1.5 16.5F1.2 7.2F0.8 12.5F1.5 7.1F0.9 6.9F0.8 7.7F1.1 6.9F0.8 7.8F1.2 8.0F1.1 4.8F0.7
32 20.2F1.7 21.4F1.7 8.6F1.3 12.4F1.2 9.2F1.3 7.4F0.9 7.5F2.2 6.5F2.3 7.0F0.8 7.4F0.9 5.0F0.9
P.K. Phillips, J.E. Heath / Comparative Biochemistry and Physiology, Part A 138 (2004) 451–457454
Fig. 2 shows the changes in Ts for the squirrel eye, ear,
head, and nose over time. Temperature of all these surfaces
increased slowly until the eyes opened at Tb 18.1 8C, thenincreased in parallel with Tb for the remainder of the arousal
period.
Fig. 3 shows changes in Ts of the squirrel body with time.
There was very little increase in Ts of these areas in early
arousal, with an anterior to posterior gradient of 1.5 8Cbeing evident in looking at flanks. Again after 80 min when
the eyes opened and Tb reached 18.1 8C, Ts of all four
surfaces increased. The anterior to posterior gradient
increased to a maximum of 5 8C. All body surface
temperatures were maintained at a constant level once Tb
reached 27 8C.Foot Ts (Fig. 4) did not begin to increase above Ta until
the eyes opened. Similar Ts was measured for each foot
until Tb reached 30 8C. At that point, an anterior to
posterior gradient was established in the feet averaging 1.6
8C and they began to be regulated at a constant temper-
ature. The tail Ts remained close to Ta throughout the
arousal session.
The mean mass of the seven marmots was 2.26F0.54 kg.
It took the larger marmots longer to arouse than the
squirrels. Mean arousal time was 2.60F1.05 h (range
1.75–4 h); mean mass-specific warming rate was
4.49F1.63 8C/h/kg. Average Tb at the beginning of arousal
Fig. 2. Surface temperatures of the head regions all increase at the same rate
as body temperature (based on t-test of similar slopes; pb0.01) once the
animal opens its eyes at Tb=18.1 8C.
was 9.4F1.4 8C (range 7.4–11.5 8C). It is likely that the
marmots were not all at the same point in their hibernation
cycle, which would account for the difference in arousal
times and the range of starting Tb’s. Figs. 5–7 show data for
a 2.37 kg male yearling marmot. Warming curves for all
marmots fit an exponential function and were significant
(range for R2s=0.911–0.992). All Tb data for the marmots
were taken from interscapular measurements, which pro-
vided more data in late arousal. The greater number of
points increased the ability to fit the data to the exponential
function.
A plateau in Tb was evident in the data for all
marmots, although the length varied between individuals
(mean duration 9.2F4.1 min). The mean interscapular
temperature at which this occurred was 20.3F1.0 8C. Inall cases, this plateau corresponded to the point at which
the animal opened its eyes, determined visually and on
the IR tapes. For the marmot shown in Figs. 5–7, this
occurred at Tb of 22.0 8C, 150 min into arousal and lasted
for 15 min.
Fig. 5 shows changing Ts of the marmot head region
over time. Eye and ear Ts increased throughout the arousal
in parallel with Tb, leveling off to euthermic values when
Tb reached 27 8C. The remainder of the head surface
increased in temperature until the end of the plateau period,
at which point it was near euthermic levels and remained
relatively constant. Ts of the nose did not increase until
Fig. 3. Comparison of flank temperature indicates a differential vaso-
constriction occurs in this species during arousal.
Fig. 4. A slight anterior to posterior gradient is evident in Ts of the feet. Tail
does not seem to be involved in heat loss.
Fig. 6. Body surfaces did not increase in temperature until the Tb plateau at
22 8C. No anterior/posterior gradient is evident. When Tb begins to rise
again, Ts of the body ceases to rise.
P.K. Phillips, J.E. Heath / Comparative Biochemistry and Physiology, Part A 138 (2004) 451–457 455
after the plateau in Tb, when it was maintained at a level
slightly below that expected for a euthermic animal
(Phillips, 1992).
Fig. 6 shows the data for the marmot body surfaces
(abdomen, back, flanks) over time. There was no meas-
urable increase in Ts of these areas until Tb reached 22 8C.At that point, with Tb remaining constant, body Ts increased
slightly in all four regions reaching a point just below
euthermic levels and was maintained.
Fig. 7 shows changes in marmot foot and tail Ts with
time. As with the body surfaces, there was no increase in Tsof the feet until the plateau stage was reached. Once Tb
reached 30 8C, foot temperatures remained constant show-
ing a small anterior to posterior gradient of 1.65 8C. As with
Fig. 5. Nose and head Ts was maintained once Tb reached 22 8C. Eye andear Ts increases at the same rate as Tb until it reached 27 8C.
the squirrels, Ts of the tail remained near Ta throughout the
arousal period.
4. Discussion
Hibernating animals use the same temperature regulatory
neurons as euthermic animals (Heller and Colliver, 1974)
and respond to changes in the preoptic anterior hypothal-
amus in the same manner whether hibernating or awake
(Wunnenberg and Kuhnen, 1990). It can be concluded that
the central neural regulator of Tb is continuously active over
the entire range of Tb experienced by the hibernator (Florant
et al., 1978). The theory that the control system remains
Fig. 7. A slight differential in foot temperature is evident. Ts is slightly less
than in a euthermic animal at the same Ta.
P.K. Phillips, J.E. Heath / Comparative Biochemistry and Physiology, Part A 138 (2004) 451–457456
active throughout hibernation as well as that set point
returns to euthermic level to allow arousal to occur has
much support (Hammel, 1967; Florant and Heller, 1977;
Florant et al., 1978) although it is still not known if set point
increases gradually or all at once. Nevertheless, any changes
in peripheral vasomotion detected by IRT in hibernators
would be using the same neural control processes as those
seen in euthermic animals. We determined when the arousal
period was concluded and ended each trial when surface
temperatures had either reached or were approaching
euthermic levels.
Although their reasoning was disputed at the time,
Lyman and Chatfield (1955) concluded that the bright pink
feet of hibernating hamsters (M. auratus) indicated the
animals were fully perfused in hibernation. The same
conclusion has been reached for the eastern chipmunk
(Tamias striatus) (Wang and Hudson, 1971) and the arctic
ground squirrel (Spermophilus parryi) (Barnes, 1989). It
can then be assumed that the ground squirrels and marmots
were fully perfused at the beginning of each arousal period.
Two possible reasons for changes in Ts are increase cardiac
output during arousal and vasomotor changes; vasoconstric-
tion followed by vasodilation of the same areas to complete
the warming process. This general sequence has been
confirmed using dilatory drugs in other species (Lyman
and O’Brien, 1960, 1972; Lyman, 1982). Increased cardiac
output contributes to the increases in blood flow in general.
As warmed blood circulates, the animal must use vaso-
motion to prevent heat loss and to warm body regions
selectively. The resulting Ts changes, as are visible by IRT,
can then be related to the animal using vasomotion.
The warming pattern was the same for both species,
although the expected differential vasoconstriction was
difficult to see in the marmot because the heavier fur on
the body tended to reduce heat loss and lower Ts. Tb
increased exponentially. The greatest increase always
occurred during bouts of severe shivering. This would
mimic previous records for arousal in eastern chipmunks (T.
striatus) in which exponential increase in Tb occurred with
the hardest shivering (Wang and Hudson, 1971). One of the
most notable differences between the two species was the
plateau in Tb that was seen in the marmots and lack of such
a plateau in the squirrels. Although the length of time when
Tb remained constant was short, it was a consistent
phenomenon in all seven marmots and one that was
conspicuously absent in all eight squirrels. The larger size
of the marmot may make it more difficult to conduct heat to
the extremities. Thus, the marmot cannot increase both Tb
and Ts at the same time and must forego one for the other.
Body surface temperatures were apparently increased
sufficiently in a few minutes in all cases after which Tb
continued to rise.
The smaller ground squirrel apparently perfuses distal
regions without needing to slow the increase in Tb. The
largest increase in Ts did not occur in either animal until the
eyes opened. Because Tb did not increase significantly in
any of the squirrels until the eyes opened, this seemed to
indicate an important step in the arousal period, and a
comparison of Ts at this same marker in the marmot seems
in order. The mean temperature at which eyes opened was
1.6 8C higher for the marmot. This could be an indication of
the smaller animal being able to warm the extremities more
easily. The vasomotor index (VMI), which reflects an
animal’s ability to regulate Ts, would be lower for the
smaller squirrel, when compared to the marmot, suggesting
the smaller animal has less overall control of vasomotion
and heat loss. Nevertheless, the VMI of the squirrel is still
higher than would be predicted for an animal of its size
(Phillips and Heath, 1995). This extra degree of control may
be helpful to the small squirrel during arousal.
Arousal time is a reflection of the size of the animals.
The larger marmot, with more body to warm, a smaller
surface area to volume ratio, lower mass specific warming
rate and lower mass specific metabolic rate, requires a
longer time to do so. Arousal time may also be affected by
the point in the cycle at which the animal was aroused.
Certainly, there is a relationship between arousal time and
the temperature at which arousal was initiated. Arousal in
mice is somewhat slower if the torpor period was fast
induced, such as by placing an animal in a warm room
(Gaertner et al., 1973). In this study, every instance, animals
that started with the lowest Tb also took the longest time to
arouse.
The responses of both species during arousal do not
appear to indicate any change in control of Ts. Although an
anterior to posterior temperature gradient was detected in
the arousing squirrels, in the marmots this was minimal at
best. Since differential vasoconstriction on arousal has been
described in several hibernators (Lyman, 1982; Lyman and
Chatfield, 1950; Wang, 1978; Wunnenberg and Kuhnen,
1990), we expect, this should be occurring in both species
here. Previous studies suggest the anterior to posterior
gradient should be smaller if the animal is aroused in a cold
room compared to one aroused at higher Ta’s (Lyman,
1982). All animals in this study remained in the cold rooms
being utilized for the hibernation season. The difference in
the IR results for these two species is, thus, difficult to
explain. The fur is much shorter on the smaller squirrels,
compared to the marmots, and their smaller size prevents
storage of heavy fat layers. It is probable that the technique
of ITR could not detect all of the vasomotor changes in the
marmot because of the good insulation provided by the fur
and fat. Further, it has been suggested that much of the
rapidly produced heat during early arousal is trapped by
vascular adjustment. There is a strong vasoconstriction from
core to periphery, and heat is not carried to the periphery.
Additional channels (vessels) would be opened only after
each layer has warmed (Wang, 1978). Any vasomotor
adjustments such as these would not be detected using IRT
but also would not affect Ts or heat exchange with the
environment. It does not mean, however, that those same
undetectable changes would not affect the internal warming
P.K. Phillips, J.E. Heath / Comparative Biochemistry and Physiology, Part A 138 (2004) 451–457 457
process. To date, no study has shown whether hypothalamic
set point increases instantly to 37 8C during arousal or is
more gradual, such as occurs during entry (Florant and
Heller, 1977; Florant et al., 1978). A different technique is
required to determine how blood flow is altered to promote
arousal in the larger, better-insulated marmot.
Acknowledgements
This research was funded by USPHS traineeship
GM07143. Allen Sanborn read an early version of the
manuscript and assisted with the initial studies. The authors
gratefully thank John Willis and Marina Marjanovic for the
use of the squirrels and cold room at the University of
Illinois and Greg Florant for his assistance and use of
marmots and facilities at Temple University.
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