522
Merriam’s Kangaroo Rats (Dipodomys merriami) Voluntarily Select
Temperatures That Conserve Energy Rather than Water
Marilyn R. Banta*
Program in Ecology, Evolution, and Conservation Biology,
University of Nevada, Reno, Nevada 89557
Accepted 1/23/03
ABSTRACT
Desert endotherms such as Merriam’s kangaroo rat (Dipodomys
merriami) use both behavioral and physiological means to conserve energy and water. The energy and water needs of kangaroo
rats are affected by their thermal environment. Animals that
choose temperatures within their thermoneutral zone (TNZ)
minimize energy expenditure but may impair water balance
because the ratio of water loss to water gain is high. At temperatures below the TNZ, water balance may be improved because animals generate more oxidative water and reduce evaporative water loss; however, they must also increase energy
expenditure to maintain a normal body temperature. Hence,
it is not possible for kangaroo rats to choose thermal environments that simultaneously minimize energy expenditure and
increase water conservation. I used a thermal gradient to test
whether water stress, energy stress, simultaneous water and
energy stress, or no water/energy stress affected the thermal
environment selected by D. merriami. During the night (i.e.,
active phase), animals in all four treatments chose temperatures
near the bottom of their TNZ. During the day (i.e., inactive
phase), animals in all four treatments settled at temperatures
near the top of their TNZ. Thus, kangaroo rats chose thermal
environments that minimized energy requirements, not water
requirements. Because kangaroo rats have evolved high water
use efficiency, energy conservation may be more important than
water conservation to the fitness of extant kangaroo rats.
Introduction
Desert organisms are challenged with obtaining enough energy
and water to survive in the face of extreme temperatures, low
* Present address: Department of Biological Sciences, University of Northern
Colorado, Greeley, Colorado 80639; e-mail: [email protected].
Physiological and Biochemical Zoology 76(4):522–532. 2003. 䉷 2003 by The
University of Chicago. All rights reserved. 1522-2152/2003/7604-2100$15.00
precipitation, and low productivity. These challenges are especially severe for endotherms, whose metabolic rates and evaporative water loss (EWL) are high (Cossins and Bowler 1987;
Withers 1992). However, desert-dwelling mammals have
evolved morphological, behavioral, and physiological traits that
allow them to reduce their energy and water demands. In many
cases these morphological, behavioral, and physiological traits
function in synchrony, facilitating the acquisition and conservation of both energy and water, but this is not always the case.
The ambient temperatures experienced by endotherms can
have dramatic consequences for energy and water conservation
(Bartholomew 1972; MacMillen and Hinds 1983). Within the
thermoneutral zone (TNZ), an endothermic animal’s metabolism is minimized. At temperatures above or below the TNZ,
metabolism increases. Therefore, one way endothermic animals
can conserve energy is by choosing temperatures within their
TNZ. However, for endotherms, temperatures within the TNZ
lead to higher rates of water loss than temperatures below the
TNZ.
The various morphological, behavioral, and physiological
traits that Merriam’s kangaroo rats (Dipodomys merriami: Heteromyidae) use to survive in desert conditions have been well
studied, and the species is considered to be highly adapted for
a desert lifestyle (Schmidt-Nielsen 1964; Brylski 1993; French
1993; Randall 1993). As a general rule, the behavior of D.
merriami is affected by ambient temperature. Most activity,
including dispersal, foraging, breeding, and territorial defense,
occurs at night when air temperatures are cooler (Randall
1993). During the day, D. merriami shuttle within their burrows
to find suitable temperatures, usually at the low end of their
thermoneutral zone, if possible (Kenagy 1973).
For kangaroo rats, the major source of water loss is EWL,
and the major source of water gain is metabolic water production (MWP). Some preformed water is also gained from
food. The majority (170%) of EWL in kangaroo rats is respiratory (French 1993); some water is also lost through urine
and feces. MWP increases as oxygen consumption (i.e., metabolic rate) increases. Hence, MWP is minimized within the
TNZ. Outside the TNZ, MWP increases in concert with metabolic rate.
While MWP is minimized in the TNZ, EWL is not. EWL
increases as temperature increases within the TNZ and continues to increase as temperature rises above the TNZ. Consequently, within the TNZ, the ratio of water production (MWP)
to water loss (EWL) is low, and animals without a supplemental
source of water are likely to be in negative water balance (i.e.,
Temperature Selection in Desert Rodents
experiencing a net loss of water). At temperatures below the
TNZ, EWL becomes uncoupled from oxygen consumption
(Bartholomew 1972; MacMillen and Hinds 1983). Hence, as
oxygen consumption and MWP increase with decreasing temperature, EWL decreases slightly (Bartholomew 1972; MacMillen 1972). Therefore, as ambient temperature decreases below the TNZ, the ratio of water intake (MWP) to water loss
(EWL) increases until the animal achieves water balance (water
gain p water loss). MWP depends not only on metabolic rate
but also on the composition of the food being oxidized. Thus,
for a given food source, there is a temperature below the TNZ
at which MWP p EWL (Bartholomew 1972; MacMillen and
Hinds 1983). At temperatures below this point of equality, the
animal can achieve even more favorable states of water balance
(i.e., MPW 1 EWL). Therefore, desert animals, such as D. merriami, are faced with a trade-off. By selecting particular environmental temperatures, D. merriami can promote either water
or energy conservation, but not both.
Physiologists have debated which selective forces have produced the extant kangaroo rat (MacMillen 1983; Hinds and
MacMillen 1985; French 1993). Some have argued that the need
to conserve water in an arid environment has driven many of
the traits we see today, while others suggest it is the need to
conserve energy in a low-productivity environment that has
led to the current phenotype. Therefore, I designed an experiment to test the competing hypotheses of water versus energy
conservation. I subjected kangaroo rats to water stress, energy
stress, both stresses, or neither stress, and then placed them in
a temperature gradient. I predicted that animals that were water
stressed but not energy stressed would choose cooler temperatures to try to conserve water. I predicted that animals that
were energy stressed but not water stressed would choose temperatures within their TNZ to try to conserve energy. I also
examined what temperatures animals would choose if they had
ad lib. energy and water available to them (no stress), or if they
were both energy and water stressed. This study was designed
to identify whether temperature selection in D. merriami is
driven by the need for water or energy conservation on a very
proximate time scale, that is, temperature selection driven by
the immediate threat of starvation or dehydration.
Material and Methods
Subjects
Thirty-two adult Dipodomys merriami were captured 80 km
northwest of Reno, Nevada, at Nightingale Hot Springs (Churchill County). I captured animals using Sherman live traps
baited with bird seed (Nevada Division of Wildlife Scientific
Collecting Permit S15716). Animals were returned to an animal
care facility at the University of Nevada, Reno and housed
individually in 47 # 26 # 20 cm polypropylene cages. Each
cage had a sand substrate and contained a can the animals
523
could use as a burrow. I provided each animal with a piece of
cotton batting to use as nesting material, but not all animals
made nests. The animals were acclimated to laboratory conditions for 3–12 wk before testing began. During this time they
were fed mixed bird seed (red and white proso, millet, sunflower seeds) ad lib., lettuce twice a week (kangaroo rats typically will not drink water), and a mealworm (Tenebrio sp.)
larva once a week. The animal care facility was maintained on
a 12L : 12D photoperiod, and the air temperature ranged between 20⬚–22⬚C.
Experimental Protocol
I randomly divided the kangaroo rats into four groups: three
groups contained eight animals and one group contained seven
animals (one sick animal was excluded from the experiment).
Each animal was tested once. The groups consisted of animals
that were energy stressed but not water stressed (“energy
stressed”), water stressed but not energy stressed (“water
stressed”), both water and energy stressed (“both stresses”), and
those that were neither water nor energy stressed (“no stress”).
These treatments were maintained throughout the training and
testing period (see below). Hulled barley seeds were provided
as the source of energy. The seeds for animals in the waterstressed treatment were oven dried at 70⬚C for 96 h to remove
preformed water in the seeds and subsequently were stored in
a desiccator until testing. Seeds for animals in the no-stress
treatment were not oven dried. Water was provided in the form
of 1.0-g pieces of lettuce (provides ∼0.95 g water).
Approximately 20 h before each animal was to be tested, I
placed it in a set of four training boxes that simulated the boxes
used in the testing apparatus (Fig. 1A). Each box had 2–3 cm
of clean sand as a substrate and contained a can the animal
could use as a burrow. Each animal was weighed and placed
in the training boxes at approximately 2200 hours and remained
in the boxes overnight. At approximately 0800 hours the following morning, the animal was removed, weighed again, and
placed into its home cage until testing began that evening.
Footprints and tail drags in the sand were used as signs that
the animal had visited each box during the night. Food and
water were either provided or withheld depending on the treatment group (Table 1). When food was to be provided, I placed
4.0 g of seeds in each of the four boxes (Table 1). Dipodomys
merriami typically eat 2–3 g of seed each night. When water
was to be provided, I placed a 1.0-g piece of fresh lettuce in
each of the four boxes.
The temperature gradient used for testing temperature choice
consisted of eight boxes arranged in two rows of four such that
each box was connected to its two nearest neighbors (Fig. 1B).
Each box was a 32.2-L cooler measuring 52 # 33 # 28 cm. The
center of the lid of each cooler was cut away and replaced with
a sheet of Plexiglas to allow light to enter the box. Two holes
524 M. R. Banta
Figure 1. The design of the temperature boxes for the training period
(A) and the testing period (B). Each box is a 32-L cooler connected
to its two nearest neighbors by a Plexiglas tube. An example of the
random placement of the eight temperatures and the starting box is
shown in the diagram of the testing apparatus.
were cut approximately 4 cm from the floor to allow the animals
access to Plexiglas tubes (3.8 cm i.d.) that connected the boxes.
Two additional holes were cut near the top of the coolers to
provide an inlet for heated air and an outlet so that pressure
would not build up inside the box. Each box had clean sand
as a substrate and contained a can that the animal could use
as a burrow. The boxes were placed inside a walk-in environmental chamber that was maintained at a constant temperature
of 8⬚C. The environmental chamber was a closed system (i.e.,
the air inside the chamber was recirculated), allowing me to
control humidity using either a dehumidifier or humidifier as
necessary. Relative humidity was measured with a probe inside
the chamber and the boxes (HR30, Omega, Stamford, Conn.)
and was converted to absolute humidity. Each box was outfitted
with a computer fan (2.78 m3/min) that blew air past a heating
element (from a 1,600-W hair dryer) into the box. The fans
circulated air within the boxes enough to create some air movement. A thermocouple positioned approximately 1–2 cm from
the surface of the sand measured air temperature in the box.
The thermocouple and the heating element were connected to
a CR-10 data logger (Campbell Scientific, Logan, Utah) that
controlled the temperature inside the box by turning the heating element off and on as needed. The temperature inside the
box was recorded every 10 min for the entire test. This system
consistently maintained air temperatures inside the boxes very
close (Ⳳ0.1⬚ to 0.5⬚C) to their set point.
The temperatures used in this experiment ranged from 10⬚
to 38⬚C in increments of 4⬚C (see below). For each animal, the
eight temperatures were randomly assigned to the boxes (e.g.,
as in Fig. 1B). The box, and hence the temperature the animal
started in, was also randomly chosen. At 1600 hours the data
logger was programmed and activated, and either the humidifier or dehumidifier was turned on (Table 1). Boxes normally
reached their designated temperatures by 1630 hours. At this
time, depending on the treatment group of the animal to be
tested, 4.0 g of hulled barley seeds (normal or oven dried),
and/or 1.0 g of lettuce were added to each of the eight boxes
(Table 1). At 1700 hours the animal being tested was weighed
and introduced into the randomly chosen start box to begin
the test (hereafter known as the starting box). The lights went
out in the environmental chamber at 1800 hours and came
back on at 0600 hours the following morning (the same photoperiod as the animal care facility). A dim light (25 W)
mounted several feet from the chambers was on during the
dark period to give the animals enough light to move within
and between boxes. Between 0830 and 0900 hours, each animal
was removed, weighed, and returned to its cage. The testing
period was divided into a 11-h-45-min period of darkness
(hereafter referred to as night) followed by a 2-h-15-min period
of light (hereafter referred to as day). The first hour of testing
(1700–1800 hours), when the lights were on, was not used for
analysis. The night and day periods were analyzed separately.
The activity of the kangaroo rats was monitored using passive
infrared motion detectors (Disc 360⬚ Ceiling Mount, Visonic,
Bloomfield, Conn.). One motion detector was attached to the
ceiling of each box such that the two entry points to the box
were clearly within the infrared beams. The status of all eight
motion detectors was checked every 2.0 s by the data loggers.
If a motion detector had been activated by the movement of
an animal, the box number and time were recorded. If a motion
detector did not detect movement, no output was generated.
For each animal, a record was obtained detailing how many
visits were made to each box, how much time it spent in a box
during each visit, and the total time spent in each of the eight
boxes. I also noted whether lettuce was left in any of the boxes
and the mass of seeds remaining in each box. I did not count
visits that were less than 12 s in duration. Consequently, out
Temperature Selection in Desert Rodents
525
Table 1: Description of the animals making up the four treatment groups
Treatment Groups—Type of Stress
Sample size
Males
Body mass (g)
Females
Body mass (g)
Training:
Seeds given?
Lettuce given?
Testing:
Seeds given?
Lettuce given?
Humidifier on?
Dehumidifier on?
Both Energy
and Water
Neither Stress
8
4
34.4 (1.95)
4
31.0 (2.01)
8
4
33.6 (3.33)
4
33.5 (1.30)
7
3
36.3 (1.66)
4
31.0 (2.41)
No
Yes
Yes (dry)
No
No
No
Yes
Yes
No
Yes
Yes
No
Yes (dry)
No
No
Yes
No
No
No
Yes
Dry
Yes
Yes
No
Energy
Water
8
4
34.5 (1.51)
4
32.0 (2.05)
Note. Air, food, and water conditions used for each treatment. Body mass is the mean (Ⳳ1 SD) at
the beginning of testing.
of the total 14-h test period (night and day combined), there
are periods of time that are unaccounted for. These short periods of time are designated “travel time.” A cutoff of 12 s was
used because the motion detectors have an 8–10-s “on” lag
time, such that when an animal triggered a motion detector as
it was moving through the box, the minimum time recorded
for the animal would be 8–10 s, even if it had only actually
spent one or two seconds in the box.
Selection of Temperatures
The ambient temperature at which endotherms move from a
state of negative water balance to a state of water balance depends on the composition of the food source (MacMillen and
Hinds 1983). The millet seeds that MacMillen and Hinds fed
the kangaroo rats (also D. merriami) in their study were similar
in composition to the barley seeds I used in this experiment.
In their study, at ambient temperatures below 16⬚C the kangaroo rats were in positive water balance (water intake 1
water loss). The TNZ for D. merriami is 29⬚–34⬚C (Dawson
1955; French 1993). Therefore, the boxes maintained at 10⬚ and
14⬚C were cool enough to put animals without supplemental
water (lettuce) into a positive state of water balance. The boxes
at 18⬚, 22⬚, and 26⬚C represented intermediate temperatures
where the animals were approaching but not quite achieving
water balance. At these five temperatures, increases in energy
expenditure would be needed to maintain body temperature.
The boxes at 30⬚ and 34⬚C should have been within the TNZ
of the animals. In the 38⬚C box, the ratio of water intake to
water loss would have been very low, leading to negative water
balance for those animals without lettuce. Because 38⬚C is above
the TNZ, animals at this temperature would need to increase
energy expenditure to avoid overheating.
Measuring Operative Temperature
Operative temperature can be measured with pelage-covered
hollow copper models (Bakken 1992). I did not have access to
operative temperature models shaped like kangaroo rats, but I
did have access to deer mouse (Peromyscus maniculatus) models
that were roughly equivalent in size to a small D. merriami and
should have provided a reasonable approximation of the operative temperature of a kangaroo rat.
To obtain operative temperatures for the eight temperature
boxes, I placed three deer mouse models in each box; one inside
the can, one near the back of the box directly below the inlet
hole for the heated air, and one at the front of the box near
the openings of the two tubes connecting each box to its two
neighboring boxes. I collected temperature data from each of
the three deer mouse models and the thermocouple every 2
min for 2 h. This procedure was done in replicate for all boxes
and the values for the two runs were combined for each box.
Statistical Analyses
All statistical analyses were conducted using SAS (release 6.12)
software (SAS Institute, Cary, N.C.). ANOVA and ANCOVA
were conducted after data were tested for assumptions of normality, homoscedasticity, and homogeneity of slopes. Logarithmic transformations were used to adjust for unequal variance
in some data sets. If body mass was likely to influence a trait,
an ANCOVA was used with body mass as the covariate. A post
526 M. R. Banta
hoc Bonferroni test for multiple comparisons was used to test
for differences between treatments.
Results
Change in Mass
Footprints and tail drags in the sand indicated that every animal
visited all four of the boxes during training. Animals quickly
learned to move from box to box through the tubes. Animals
that were deprived of energy, water, or both energy and water
experienced a significant loss in mass in the training boxes
(paired t-tests, all P ! 0.01 ). Animals with both food and water
tended to gain mass but not significantly so (paired t-test,
P 1 0.05; Fig. 2). Initial body mass was not a significant covariate (F1, 26 p 0.24, P p 0.625), so a single-factor ANOVA was
used to test for treatment differences in change in mass. There
were significant differences in the change in mass between treatment groups during training (F3, 27 p 33.12 , P ! 0.001). A Bonferroni test indicated that animals in the no-stress treatment
gained significantly more mass than animals in the waterstressed and both-stresses treatments (P ! 0.001 for both tests).
The difference between the animals in the no-stress treatment
and the energy-stressed treatment was marginally significant
(P p 0.054). The energy-stressed animals lost significantly less
mass than animals in either the water-stressed or both-stresses
treatments (P ! 0.001 for both tests). There was no difference
in change in mass between the water-stressed and both-stresses
treatments.
During testing, the animals showed the same trend in mass
gain or loss as they did during training (Fig. 2). As with the
training period, body mass was not a significant covariate
(F1, 25 p 1.39, P p 0.249), so a single-factor ANOVA was used
to test for treatment differences in change in mass. There was
a significant change in mass between treatment groups during
the testing period (F3, 26 p 42.04, P ! 0.001). A Bonferroni test
indicated that all groups were significantly different from each
other except the energy-stressed and both-stresses treatments.
Activity
During the testing period, not all animals explored all the boxes.
In the energy-stressed and both-stresses treatments, all eight
animals entered all eight boxes at some point during the test.
In the water-stressed treatment, seven of eight animals entered
all eight boxes and one animal never left its starting box (26⬚C).
However, in the no-stress treatment, only three of seven animals
entered all eight boxes. Three animals spent the entire test
period in their starting boxes, and one animal moved only
between its starting box and one adjacent box. The temperatures of the starting boxes of the three nonmoving animals
were 10⬚, 14⬚, and 34⬚C. The final animal moved between the
18⬚ and 26⬚C boxes (starting box was 26⬚C). I used a G-test
to examine whether the frequency of movement between boxes
Figure 2. The mean change in mass (⫹1 SD) for each treatment group
during the training and testing periods. Negative means indicate a loss
in mass. Positive means indicate a gain in mass. An asterisk indicates
a change in mass significantly different from 0 for that treatment group.
was independent of the treatment group. The G-test was significant (x 32 p 7.81, P p 0.018), indicating that frequency of
movement depended on the treatment group. The animals with
both seeds and lettuce in all boxes (no stress) remained in their
starting box, regardless of the temperature, significantly more
often than the animals in the other three treatment groups.
Temperature Selection
The mean proportion of time spent in the various temperature
boxes during the night (Fig. 3) and day (Fig. 4) periods was
similar among the treatment groups. Note that in all groups,
animals spent a large amount of time in the hottest (38⬚C) box
during both the night and day periods, but especially during
the day.
By multiplying the proportion of time an animal spent in a
single box by the temperature of that box and then summing
these values across all eight boxes, I obtained a mean temperature for each animal during the day and the night periods
(Table 2). The mean temperatures selected by the animals during the night were not significantly different between treatment
groups whether I included all 31 animals (ANOVA: F3, 27 p
2.32, P p 0.10) or excluded the five nonmoving animals
(F3, 22 p 0.34, P p 0.80).
During the night, the animals were quite active. The number
of visits to a single box ranged from 0 to 180. Excluding the
five nonmoving animals, kangaroo rats visited each box an
average of 30.7 times during the course of the night. For these
26 animals, the mean length of each visit was 191 s.
During the day, the kangaroo rats tended to pick a single
box and then settle there for the duration of the day period.
When I removed the animals from the temperature gradient
Temperature Selection in Desert Rodents
527
Figure 3. The mean percent of time (⫹1 SD) that each treatment group spent in each of the eight temperature boxes during the night (active)
period. The night period was 11 h 45 min. Trav represents travel time, periods of time when the animals spent less than 12 s in a box (i.e.,
were moving through boxes quickly).
they were almost always resting inside the can in the box where
they had spent the bulk of the day period. As was the case
during the night period, there were no significant differences
in the mean temperatures selected by any treatment group when
all animals were included (F3, 27 p 1.29 , P p 0.30 ) or when the
five nonmoving animals were omitted (F3, 22 p 0.69, P p 0.57;
Table 2). Individual kangaroo rats chose significantly higher
temperatures during the day period than during the night period (paired t-test: t 30 p 3.25, P p 0.003).
Nineteen animals visited all eight boxes at some point during
the test but did not move at all during the final 60 min of the
day period. These animals presumably experienced all eight
temperatures and then chose the box where they would rest
during their inactive period. Of these 19 animals, 11 settled in
the 38⬚C box, five settled in the 34⬚C box, and one each settled
in the 30⬚, 26⬚, and 14⬚C boxes. The animal in the 14⬚C box
was torpid.
Food Consumption
Only animals in the water-stressed and no-stress groups received seeds during the test period. The water-stressed and nostress animals ate 1.50 Ⳳ 0.28 g and 2.47 Ⳳ 1.01 g (mean Ⳳ
SD) of seeds, respectively. I tested for differences in food consumption using an analysis of covariance (ANCOVA) with body
mass at the beginning of the test period as the covariate. The
covariate was significant (F1, 12 p 7.78 , P p 0.016). After accounting for differences in body mass, the animals in the no-
stress treatment ate significantly more than the water-stressed
animals (F1, 12 p 5.53, P p 0.037). However, the seeds the water-stressed animals were given had been dried to remove preformed water, and the drying process reduced the mass of the
seeds by ∼10%. To account for this difference in seed mass that
would not have contributed to energy intake, I subtracted 10%
from the mass of seeds eaten by each no-stress animal and then
tested for differences in food consumption. Body mass was a
significant covariate (F1, 12 p 7.68 , P p 0.017), and after adjusting for body mass, the no-stress group still ate significantly
more than the water-stressed group (F1, 12 p 5.54, P p 0.037).
Operative Temperature
The mean temperatures measured by the three deer mouse
models for these trials (operative temperature) are summarized
in Figure 5. In the two warmest boxes, the operative temperatures were between 2⬚ and 6⬚C cooler than the temperature
measured by the thermocouple. The model at the front of the
box near the connecting tubes was always cooler in the warm
boxes and warmer in the cool boxes than the other two models.
Discussion
Night Activity
During their active phase, kangaroo rats tended to choose temperatures near the low end of their TNZ, regardless of the
treatment (Table 2). The mean temperatures chosen by animals
528 M. R. Banta
Figure 4. The mean percent of time (⫹1 SD) that each treatment group spent in each of the eight temperature boxes during the day (inactive)
period. The day period was 2 h 15 min. Trav represents travel time, periods of time when the animals spent less than 12 s in a box (i.e., were
moving through boxes quickly).
in all four treatment groups ranged between 24.9⬚ and 31.3⬚C
(Table 2). The five stationary animals skew these mean temperatures downward for the no-stress (n p 4 ) and waterstressed (n p 1) treatments. When these five animals were removed, the range of temperatures selected by the four treatment
groups was much narrower (30.3⬚–31.5⬚C; Table 2).
The TNZ for Dipodomys merriami is 29⬚–34⬚C, and the mean
temperatures chosen by all four treatments lie close to the lower
end of this range. This result suggests that regardless of whether
these animals were experiencing water-stress, energy-stress,
both stresses, or neither stress, they preferred to remain at
temperatures within but near the cool end of their TNZ.
Choosing temperatures within the TNZ allows mammals to
conserve energy. However, within the TNZ, EWL is high and
MWP is low, and without supplemental water, negative water
balance is the consequence. EWL increases with increasing ambient temperature within and above the TNZ. Consequently,
with no difference in energy expenditure, choosing temperatures at the low end of the TNZ would conserve more water
than choosing temperatures at the high end of the TNZ. Because animals in all four treatment groups chose energy-conserving rather than water-conserving temperatures, it appears
that energy conservation may be driving temperature selection,
even when water but not energy is limited. A few studies suggest
that energy conservation may be more important than water
conservation for this species. On a seed diet that produces
sufficient metabolic water (i.e., high in carbohydrate, low in
protein), D. merriami can survive indefinitely without supple-
mental water (Schmidt-Nielsen et al. 1948; Hulbert and
MacMillen 1985). Seeds can be stored in the animal’s burrow,
where humidity is higher than on the desert surface, allowing
the seeds to absorb water from the air (Schmidt-Nielsen 1964).
Dipodomys merriami survived on air-dried barley seeds alone
when the absolute humidity was above 2.2 mg H2O/L air
(Schmidt-Nielsen and Schmidt-Nielsen 1951). Using a dehumidifier, I attained an absolute humidity this low within the
environmental chamber. In addition, by oven drying the seeds,
I removed the preformed water in the barley seeds offered to
the water-stressed animals. Therefore, the animals in the waterstressed treatment should not have been capable of surviving
indefinitely without supplemental water. Animals in the waterstressed treatment lost mass during the training and testing
periods (Fig. 2), which supports this premise. However, it is
unlikely that the wild seeds would have all preformed water
removed or that humidity would consistently be this low, especially within the burrow. Therefore, sufficient water may not
be difficult for wild D. merriami to obtain.
Most of the kangaroo rats in this study were active throughout the entire night period. However, five animals either did
not move from their starting box at all or moved only into
one adjacent box. These stationary animals belonged to two
treatment groups: one to the water-stressed treatment and four
to the no-stress treatment. Both of these treatment groups had
seeds available in all eight boxes. It seems that if the animals
had a source of readily available food, they were less likely to
explore, regardless of the temperature of the box they were in.
Temperature Selection in Desert Rodents
529
Table 2: Temperatures selected by each treatment group for night and day periods
Night Period
Type of Stress
All Animals
Energy
Water
Energy and water
Neither
30.4
29.9
31.3
24.9
Ⳳ
Ⳳ
Ⳳ
Ⳳ
3.3
2.2
2.1
9.6
Day Period
Movers
(8)
(8)
(8)
(7)
30.4
30.5
31.3
31.6
Ⳳ
Ⳳ
Ⳳ
Ⳳ
All Animals
3.3
1.6
2.1
2.0
(8)
(7)
(8)
(3)
34.4
34.2
31.9
28.1
Ⳳ
Ⳳ
Ⳳ
Ⳳ
2.9
4.8
8.5
9.8
Movers
(8)
(8)
(8)
(7)
34.4
35.3
31.9
36.2
Ⳳ
Ⳳ
Ⳳ
Ⳳ
2.9
3.8
8.5
2.3
(8)
(7)
(8)
(3)
Note. Table shows mean temperatures (⬚C) Ⳳ1 SD. Means are given for all animals (n p 31 ) and for the subset
of animals that left their starting box and visited all eight temperature boxes (n p 26 ). Sample sizes for each
treatment group are in parentheses.
All the animals in the two treatment groups that did not have
seeds available visited all eight boxes repeatedly, presumably in
an attempt to forage. Despite the fact that animals in these two
groups were energy stressed, they chose to expend energy foraging rather than to conserve energy by restricting movement.
Unless the kangaroo rats in this group had some way of realizing
that they would never obtain food while in the thermal gradient,
this seems like a reasonable behavioral response. The Australian
marsupial Sminthopsis macroura also did not reduce activity
levels when food was restricted (Song et al. 1998), although
individuals increased the length of torpor bouts in response to
food restriction. Dipodomys merriami do not typically use torpor as an energy conservation strategy (French 1993); however,
one animal in the both stresses treatment did come to rest in
a cool (14⬚C) box and entered torpor.
Day Activity
The mean temperatures selected by individuals during the day
(regardless of treatment group) were significantly higher than
temperatures selected at night. The tendency to select higher
temperatures during the inactive period has been documented
in several nocturnal (e.g., golden hamsters, rats, flying squirrels,
fat-tailed gerbils) and diurnal (e.g., degus, tree shrews) species
(Gordon 1993; Refinetti 1996, 1998a, 1998b). Because body
temperature in endotherms is higher when the animals are
active, this 180⬚ phase shift between body temperature and
temperature selection is thought to reduce the amplitude of
daily body temperature rhythms (Refinetti 1995, 1998a).
Selection of High Ambient Temperatures
In this study, with the exception of the animals in the both
stresses treatment, the mean daytime (resting) temperatures
selected were near or even above the upper end of the published
TNZ for D. merriami (Table 2). Many animals spent the majority or all of the day period in the hottest temperature box
(38⬚C), and even at night, individuals spent large amounts of
time in this box as well. In terms of conserving energy and
water, this is the one box that the animals should have avoided
as both energy and water demands are high at this temperature.
At least two explanations may account for why the animals
chose to spend so much time in the 38⬚C box during both the
day and night periods: (1) the animals shifted their TNZ such
that the 38⬚C box fell close to or within the shifted TNZ, and
(2) the temperature the animals were experiencing inside the
boxes differed from the air temperature measured by the thermocouples in the boxes.
Shift in TNZ. It is generally believed that mammals thermoregulate around a set point designed to maintain a constant
core temperature (e.g., 37⬚C in humans) and that this set point
can be altered (Cossins and Bowler 1987). Torpor and hibernation are examples of set point alterations. If the set point is
increased, the animal attempts to regulate its body temperature
at a higher temperature because the old set point is perceived
as hypothermic (Cossins and Bowler 1987). Selecting warmer
temperatures is one means of elevating body temperature (Gordon 1983). As ambient temperature increases, skin temperature
increases, and the temperature gradient between the skin and
the air is reduced (Crawshaw and Stitt 1975). A decrease in
this temperature gradient leads to a decrease in heat loss from
the animal. This reduced gradient for heat loss allows the animal
to retain heat and increase core body temperature. Therefore,
one way that an animal can maintain a higher body temperature
without increasing metabolic demands is to shift the TNZ upward such that the animal selects higher temperatures. Likewise,
a decrease in the set point could then lead to a downward shift
in the TNZ because less heat is required to maintain the lower
set point, and cooler ambient temperatures would increase the
gradient between the skin and the air, allowing the animal to
lose heat more easily. Fever, acclimation temperatures, photoperiod, and pregnancy have all been shown to cause shifts
in the set point of rodents (Bligh 1973; Gwosdow and Besch
1985; Long et al. 1990; Eliason and Fewell 1997; Haim et al.
1998). Pregnancy was not a possible cause for a shift in set
point in this study. Fever is associated with a temporary increase
in set point that is caused by pyrogens released in response to
infections (Cossins and Bowler 1987). There were no indications that any of the kangaroo rats in this study were sick or
530 M. R. Banta
Figure 5. Comparison of temperatures measured by a thermocouple and three deer mouse–shaped hollow copper models. The thermocouple
measured air temperature, and the deer mouse models measured operative temperature for ∼2 h in each of the eight temperature boxes. Data
are means (⫹1 SD) of combined data for two 2-h runs.
diseased, hence it is unlikely that fever caused an upward shift
in the TNZ.
Acclimation temperature has also been linked to a shift in
TNZ. Laboratory rats acclimated to temperatures within their
TNZ had a TNZ that was wider (20⬚–29⬚C) than rats acclimated
to temperatures below their TNZ (22⬚–27⬚C; Gwosdow and
Besch 1985). The kangaroo rats in this study were housed at
temperatures between 20⬚–22⬚C, well below their TNZ. Therefore, if the kangaroo rats were acclimated to temperatures in
the housing facility, they may have experienced a shift in their
TNZ.
Finally, photoperiod has also been linked to a shift in TNZ.
Three species of rodents acclimated to long (16L : 8D) and then
short (8L : 16D) photoperiods experienced a downward shift
in their TNZ during the short exposure relative to the long
exposure (Haim et al. 1998). The kangaroo rats in this study
were acclimated to a 12L : 12D photoperiod, the same as the
kangaroo rats in studies that determined the thermoneutral
zones in this species (Dawson 1955; Hinds and MacMillen
1985). Therefore, the kangaroo rats in this study probably did
not experience a shift in their TNZ in either direction due to
photoperiod.
In summary, while most mechanisms known to shift TNZ
could not have been factors in this study, it is possible that
some mechanisms could have caused a shift in the TNZ of the
kangaroo rats. Even a small shift upward may have been sufficient to cause the kangaroo rats to spend substantial time in
the 38⬚C box.
Temperatures Experienced in the Boxes. Based on the design of
the thermal gradient, I thought it might be possible that the
temperatures the kangaroo rats experienced inside the boxes
were not the same as the air temperatures recorded by the
thermocouples (Porter 1969). In evaluating the thermal decisions made by the kangaroo rats in this study, it is important
to distinguish between air temperature and the thermal environment. Air temperature is a potentially misleading indicator
of the thermal environment, particularly because it does not
account for the effects of wind speed and radiation (Bakken et
al. 1985). A better way to assess the thermal environment than
measuring air temperature is to measure operative temperature
(Bakken and Gates 1975; Bakken 1992). For ectotherms, operative temperature, the equilibrium temperature reached by
an animal in a given thermal environment, provides an inte-
Temperature Selection in Desert Rodents
grated measure of the thermal environment. For endotherms,
operative temperature does not fully integrate all aspects of the
thermal environment, but it does provide a better indicator
than air temperature of how hot or cold the environment is
for the animal.
The operative temperature results suggest that the thermal
environment the kangaroo rats experienced in the 38⬚C box
was cooler than the air temperature indicated, perhaps cool
enough to allow the animals to be at the upper end of their
TNZ in this box. The thermal environment in the 34⬚C box
was almost certainly within their TNZ.
Conclusions
Animals attempting to thermoregulate may choose behavioral
rather than autonomic means to maintain body temperature
because behavioral responses can be faster and less energetically
demanding (Bligh 1973; Gordon 1985; Yoda et al. 2000). If
animals use behavior to thermoregulate, then it seems likely
that they may also use behavior to facilitate energy and water
conservation as well. That is, it may be quicker and less costly
for kangaroo rats to conserve energy and water behaviorally by
selecting appropriate temperatures than to use autonomic
means such as forming a concentrated urine or undergoing
torpor.
This study was designed to test whether energy- or waterstressed animals chose temperatures that conserve water or
energy. Regardless of whether they were energy-stressed, waterstressed, or energy- and water-stressed, most animals selected
mean temperatures that were probably within their TNZ. Although, during the day, some individuals selected temperatures
that may have been above the TNZ. My results suggest that
energy conservation, not water conservation, drives temperature selection in this species, at least over a very proximate
time scale, one that may involve life or death (due to starvation
or dehydration) decisions. Kangaroo rats seem to be more sensitive to immediate shortages of food than of water.
It is also interesting to speculate on what these results may
suggest about energy and water conservation over longer, evolutionary time. Kangaroo rats are well-known for their remarkable ability to conserve water, but they may not regularly
experience water stress. As the southwestern United States and
northwestern Mexico became increasingly arid and primary
productivity decreased in the later Tertiary, kangaroo rats were
faced with decreasing food and water resources (MacMillen
1983; Hinds and MacMillen 1985). While they have evolved
morphological, behavioral, and physiological traits that allow
them to conserve both water and energy, this study suggests
that extant kangaroo rats are able to conserve water so well
that water conservation no longer drives temperature selection.
The selection of temperatures within the TNZ by all treatment
groups and the increased activity (presumably to forage) by the
animals deprived of food supports the idea that energy con-
531
servation is more important for kangaroo rats than water
conservation.
Acknowledgments
I would like to thank L. Christensen, R. Duncan, T. Grothaus,
Dr. S. Jenkins, K. Nussear, and Dr. C. R. Tracy for assistance
in designing and constructing the thermal gradient. Special
thanks to Dr. J. Hayes for providing laboratory space, equipment, and the motion detectors, as well as for valuable comments on the manuscript. Two anonymous reviewers also improved the manuscript. Funding was provided by Grants-in-Aid
of Research from the American Society of Mammalogists. All
experiments were approved by the University of Nevada Institutional Animal Use and Care Committee and conducted
under Animal Care and Use Protocol A98/99-36.
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