comparison of surface temperature in 13-lined ground squirrel (spermophilus tridecimlineatus) and...

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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 (T s ) 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 (T s ) 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 (T b ). All squirrel T s ’s remained low as T b rose to 18 8C, at which point, eyes opened, squirrels became more active and all T s ’s rose parallel to T b . Marmot T s remained low as T b rose initially. Each marmot showed a plateau phase where T b remained constant (mean T b 20.3F1.0 8C, duration 9.4F4.1 min) during which time all T s ’s rose, and then remained relatively constant as T b again began to rise. An anterior to posterior T s 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, 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 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). Comparative Biochemistry and Physiology, Part A 138 (2004) 451– 457 www.elsevier.com/locate/cbpa

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Page 1: Comparison of surface temperature in 13-lined ground squirrel (Spermophilus tridecimlineatus) and yellow-bellied marmot (Marmota flaviventris) during arousal from hibernation

www.elsevier.com/locate/cbpa

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

Page 2: 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 / 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

Page 3: Comparison of surface temperature in 13-lined ground squirrel (Spermophilus tridecimlineatus) and yellow-bellied marmot (Marmota flaviventris) during arousal from hibernation

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

Page 4: Comparison of surface temperature in 13-lined ground squirrel (Spermophilus tridecimlineatus) and yellow-bellied marmot (Marmota flaviventris) during arousal from hibernation

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.

Page 5: Comparison of surface temperature in 13-lined ground squirrel (Spermophilus tridecimlineatus) and yellow-bellied marmot (Marmota flaviventris) during arousal from hibernation

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.

Page 6: 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 / 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

Page 7: 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 / 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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