Using temperature-sensitive radio transmitters on collars,
the skin temperatures of fourteen golden-mantled ground squirrels (Spermophilus
lateralis) were measured for the non-active time periods before dawn
and after dusk to determine whether periods of torpor, when Tb (body
temperature) < 30°C were used during the summer days preceding
winter hibernation. Four of the fourteen squirrels showed at least one
state of torpor during this time period. The reasons for the squirrels’
use of this daily torpor during the summer are not completely clear.
Radio telemetry was also used to find the burrow locations for each
squirrel. Using a geographical positioning system (GPS), the burrows
were mapped. Then, nightly tracking determined if the squirrels moved
from their original burrow. Seven of the fourteen squirrels moved from
their original burrows. Two of these seven moved from their original
burrows to a new burrow at which they remained. One squirrel moved from
its original burrow to a second burrow, and then it moved from this
burrow to a third burrow at which it remained. The remaining four squirrels
moved frequently between two to three burrows. The reasons for the squirrels’
use of more than one burrow are not clear and the distances traveled
are not consistent among the seven that move. All four of the squirrels
that used daily torpor lived in more than burrow. Statistical analysis
of the torpor use and burrow movement was used to determine whether
there was a substantial difference between the male and female squirrels,
however due to the small number of squirrels, no conclusions could be
Many mammals use hibernation as a way to survive in extreme
environments where the temperatures are very high or low and where the
food and/or water are scarce. At an elevation of 3,810 m, the temperatures
in the White Mountain range of California can be as low as -23.7 °C
and the winds can be 23 m/s in mid-winter months (McCurdy, G. 2004.)
The golden-mantled ground squirrel (Spermophilus lateralis) that lives
near Mt. Barcroft, south of White Mt. Peak, uses hibernation for about
8 months of the year, from late August to April, to survive the harsh
winters. Like many hibernators, the ground squirrels reproduce immediately
following spring emergence giving birth to 1 litter per year of 4–6
young born in early summer, after gestation of 26–33 days (Kunz
et al. 1998; Michener 1998). During the brief summer months, the ground
squirrels spend most daylight hours foraging in order to fatten for
During this hibernation period, the squirrels undergo
bouts of torpor, which is characterized by the rapid decline in metabolism
and body temperature (Tb). Rates of metabolism during deep torpor are
typically less than 3% of euthermic, or non-torpid, rates at the same
ambiant temperature (Ta), or environmental temperature (Geiser 1988;
Heldmaier and Ruf 1992.) Torpor is defined for the ground squirrel to
be when the squirrel’s Tb < 30°C (Barclay et al. 2001.)
While many studies have focused on the physiological changes in the
squirrels during the hibernation period, little is known about the initial
onset of torpor.
One of the goals of this study was to determine how the
golden-mantled ground squirrels immerge, or enter, the torpid state
in the first bout of their hibernation. One of the hypotheses tested
in this study was that the squirrels enter hibernation gradually by
using daily torpor (when Tb <30°C) during the summer nights in
preparation for hibernation. In this study Tb was determined by measuring
the squirrels’ skin temperature (Tsk.) Measuring Tsk is a less-invasive
way to measure Tb of an animal because it only needs to touch the skin
of the animal rather than be surgically implanted.
The second goal of this study was gain a better understanding
of the burrowing behavior of the squirrels. The specific questions that
were asked were if the squirrels live in one or more burrows and if
the squirrels have different burrows for the summer and winter. It was
hypothesized that the squirrels move from a summer burrow to a more
sheltered winter burrow prior to hibernation.
Fourteen AVM Instruments Co. model G3-1V radiocollars
were set to send signals with frequencies ranging from 160.073-161.651
MHz. These collars were placed on eight female and six male golden-mantled
ground squirrels. Each collar was individually calibrated to measure
the squirrels’ Tsk to the nearest 0.5°C. After the squirrels
were released with their collars, the signals were located using the
AVM Instruments Co. model LA 12-Q radiotelemetry receiver and an antenna.
The time for the collars to send 50 temperature-dependent signals was
recorded for each squirrel. The shorter the time period was for 50 signals,
the higher the Tsk. The recorded time was used to calculate the Tsk
for each squirrel. The exact time of day when each tracking occurred
was recorded in order to know Ta at that time.
The majority of tracking and recording of the signals
occurred before sunrise (5:30am-6:00am) and after sunset (7:45pm-8:15pm),
when the squirrels would be in a resting state. By recording the temperatures
at these times, the normothermic, or non-torpid, Tsk for each squirrel
was determined (Barclay et al. 2001.) Therefore a period of torpor,
when Tb < 30°C, would be noticed as comparably different. The
squirrels’ Tsk was also recorded for various times throughout
the day and night in order to determine the normothermic temperatures
during activities such as foraging and sleeping.
Radio telemetry was also used to locate the squirrels
in their burrows. Using the attenuator of the receiver, which decreased
the frequency/volume of the signal, the exact location of each squirrel
in its burrow could be found. Once the burrow site had been located
for each specific squirrel, it was marked with a visible flag. Then,
using the Garmin GPS 12XL, Version 2.01 N. America City Data mapping
unit, the latitude, longitude, and altitude was recorded for each burrow
site. The burrows were located each night. This information about each
burrow was used to detect if a squirrel stayed in the same burrow or
moved to a different burrow.
The characteristics of each burrow were recorded: altitude,
incline, direction that the burrow hole was facing, and surrounding
environmental elements. These characteristics allowed for the comparison
between two different burrows that a certain squirrel lived at.
Of the fourteen squirrels that skin temperatures were
recorded for, four decreased their Tsk to below 30°C at least once
in the period of days between July 14th and August 9th, 2004. On the
mornings of July 17th and 18th, Squirrel no. 2 decreased its Tsk to
29.6°C and 28.28°C with a long photoperiod (14.2:9.8-h light-dark
cycle) and with the air temperature at 6.9 and 7.7°C. In between
these two separate bouts of daily torpor, the squirrel raised its Tsk
to 35.5°C. The temperature changes of Squirrel no. 2 are demonstrated
in Figure 1 in Appendix A.
During the entire day of July 15th, squirrel no. 4 was
in a torpid state. This squirrel lowered its temperature to 28.78°C
in the morning and 27.98°C in the evening. In a separate instance
on August 5th, this squirrel decreased its Tsk to 29.58°C. The changes
in the Tsk of Squirrel no. 4 are demonstrated in Figure
Squirrel no. 5 decreased its Tsk to 27.89°C on the
night of July 18th. This decrease in temperature is demonstrated in
Squirrel no. 13 also decreased its Tsk< 30°C to
29.7°C during the morning of July 16th. This decrease in Tsk is
demonstrated in Figure 1.
The majority of the squirrels’ lower Tsk’s,
including when Tsk < 30°C, occurred during the early hours around
5:00-6:00 AM when the Ta ~7-8. The skin temperatures for all 14 squirrels
are presented over a typical 48-hr period in Figure
The burrowing behavior of the squirrels was researched
by locating the squirrel each night over a two-week period. During this
time period, seven of the fourteen squirrels moved from their original
burrow. Two squirrels moved from their original burrows to a new burrow
at which they remained. One squirrel moved from its original burrow
to a second burrow. Then the squirrel moved from this burrow to a third
burrow at which it remained. Three squirrels moved frequently between
2 different burrows. Lastly, one squirrel moved frequently between 4
burrows. Two of the female squirrels shared burrow locations for two
of their burrows.
Squirrel no. 2 was originally located at N 37°34.848’,
W 118°14.339’ on July 20th. Later, on July 28th this squirrel
was found at a different burrow located 16m from the first burrow. This
squirrel remained at the second burrow during the remainder of the study.
Squirrel no. 13 was originally located at N 37°34.995’, W
118°14.250’ on July 27th. This squirrel remained in this burrow
until August 2nd when it moved 150m to a new burrow at N 37°35.067,
W 118°14.201’ where it remained.
Squirrel no. 5 was originally found at N 37°35.079’,
W 118° 14.104’ during the night of July 21st. It remained
in this burrow until July 30th, when it moved 80m to a new burrow located
at N 3735.120, W 118°14.092’. The squirrel remained in this
second burrow until August 1st when it moved 200m to a third burrow
located at N 37°35.135’, W 118°14.201’. This squirrel
remained in its third burrow for the remainder of the study.
Squirrel no. 4 was originally found on July 21st under
the garage of the station at N 37°35.022’, W 118°14.162.
It remained at this burrow until July 31st when it moved 20m to N 37°35.032’,
W 118°14.170. Then the squirrel made two more moves to and from
the first and the second burrow.
Squirrel no. 1 was originally located at N 37°34.746’,
W 118°13.919’, south of a large boulder hill on July 20th.
It remained at this burrow until July 29th when it moved 250m to the
north side of the boulder hill at N 37°34.873’, W 118°13.964.
Then on August 3rd, this squirrel moved back to the first burrow only
to return to the second burrow on August 4th to remain for the rest
of the study.
Squirrel no. 7 was originally located at N 37°34.986’,
W 118°14.166’ within the rock formation of the east side of
the bridge over a ditch along the road to Barcroft on July 22nd. The
squirrel remained there until the night of July 30th when it moved to
a burrow located at N 37°34.938’, W 118°14.202’under
a boulder of a tundra field. On August 4th, this squirrel returned to
its original burrow in the bridge only to return to its second burrow
on August 5th. Once again, on August 7th, this squirrel returned to
its original burrow, returning to its second burrow on August 8th.
Squirrel no. 12 was originally located on July 27th at
N 37°34.981’, W 118°14.161’ underneath a row of
old, wooden telephone poles. The squirrel remained at this burrow until
July 30th when it moved 20m to a burrow located at N 37°34.981’,
W 118°14.160’. On August 2nd, this squirrel once again moved
back to its original burrow. Then on August 4th, this squirrel moved
100 m to N 37°34.938’, W 118°14.200’ for its third
burrow. On August 5th, the squirrel moved back to its second burrow.
On August 6th, the squirrel moved to a fourth burrow near the second
burrow, on the western edge of the bridge at N 37°34.986’,
W 118°14.166’. On August 7th, this squirrel once again returned
to its original burrow location under the telephone poles. Lastly, on
the night of August 9th, this squirrel moved to its fourth burrow on
the western edge of the bridge.
The distances traveled by the seven squirrels that moved
from their original burrow are presented in Figure
3: Comparison of distances travelled by moving squirrels
The remaining seven squirrels: Squirrel no.’s 14,
6, 9, 8, 10, 3, and 11 did not move from their original burrow.
The seven squirrels that moved included five of the eight
female squirrels and three of the six male squirrels. All four squirrels
which decreased their Tsk < 30° (squirrels 2, 4, 5, and 13),
moved from their original burrows.
Because four of the fourteen squirrels have decreased
their Tsk < 30°C, analysis concludes that these squirrels were
in a period of torpor during these low temperatures (Barclay et al.
2001). One of the squirrels that used daily torpor, Squirrel no. 2,
was in a torpid state during the mornings of July 17th and 18th. Because
this squirrel had a normothermic period during the early evening readings
of July 17th raising its Tsk to 35.5°C, it can be concluded that
this squirrel had two periods of torpor. This data and other data of
the other squirrels show that squirrels have the ability to decrease
and increase their Tb rapidly, demonstrating their control over their
Of the squirrels that showed daily torpor, one was male
and three were female.
Statistical analysis was used to determine if there was
a clear relationship between the sex of the squirrel and the use of
torpor. However, because the number of squirrels that used daily torpor
was small, no clear connection was found.
Although the ambiant temperature (Ta) was recorded, there
was not a clear relationship between it and the use of torpor. The lowest
Tsk’s were recorded at the morning readings possibly because the
squirrels begin decreasing their temperature through the previous night
and raise their temperature through the day, which would explain the
higher temperatures during the nightly readings ~8:00PM.
Because only four of the fourteen squirrels used torpor,
it may not be a requirement to use daily torpor in order to prepare
for the upcoming winter hibernation. Due to the lack of time, this study
ended before the squirrels immerged into hibernation. Thus, it is not
known whether the daily torpor is directly related to the winter hibernation,
such as a preparation mechanism, or if it is used independently during
the summer months. It is very interesting that these squirrels use a
form of daily torpor infrequently. The data indicates that some squirrels
keep their Tb at a relatively consistent temperature while others increase
and decrease their temperatures to a large degree from day to day.
The golden-mantled ground squirrel has the ability to
control its body temperature ranging from its normothermic temperature
at ~ 37°C - 4°C. When compared to endotherms, which regulate
their body temperatures within a few degrees, the temperature control
and range of the squirrels are impressive.
The data shows that seven of the fourteen squirrels have
moved at least once from their original burrows. Three of the moving
squirrels have moved permanently, never returning to previous burrows.
The remaining four moving squirrels move frequently between the 2-3
burrows. Because the other seven squirrels have not moved from their
original burrows, it must not be a requirement for hibernation. Also,
because four of the squirrels move back and forth from one burrow to
another, the squirrels can live in more than one burrow. Two of the
squirrels live under buildings and two others live within the built
bridge along the road over the ditch. Because many of the squirrels
live within areas that have high human activity, this suggests that
the squirrels are not greatly disturbed by humans and may use these
locations for the greater protection offered by these structures from
the cold conditions experienced throughout the year.
The characteristics of each burrow were compared to see
whether the squirrels were choosing a second burrow for a specific reason.
However, the data did not explain why the squirrels chose the sites
for their burrows. The differences between the two or three burrows
that the seven squirrels lived in, varied with each squirrel. There
was not a consistent change in burrow characteristics.
Statistical analysis was used to determine if there was
a clear relationship between the sex of the squirrel and having more
than one burrow. However, because the number of squirrels that moved
was small, no clear connection was found.
Frank, Craig – Fordham University
The National Science Foundation for the grant, IBN-036330,
which covered all costs in this study
1 – Squirrels no. 2, 4, 5, and 13 decreasing Tsk < 30°C