Ethology
Kangaroo Rats Remodel Burrows in Response to Seasonal
Changes in Environmental Conditions
Andrew J. Edelman
Department of Biology, University of New Mexico, Albuquerque, NM, USA
Correspondence
Andrew J. Edelman, Department of Zoology
and Physiology, University of Wyoming,
Laramie, WY 82071 USA.
E-mail: [email protected]
Received: August 11, 2010
Initial acceptance: December 5, 2010
Final acceptance: February 14, 2011
(D. Zeh)
doi: 10.1111/j.1439-0310.2011.01890.x
Abstract
Burrow architecture enhances important animal functions such as food
storage, predator avoidance, and thermoregulation. Occupants may be
able to maximize fitness by remodeling burrows in response to seasonal
changes in climate and predation risk. My objective was to examine
how banner-tailed kangaroo rats (Dipodomys spectabilis) modify the number of burrow entrances in response to seasonal conditions. For 3 yr, I
monitored fluctuations in number of burrow entrances in kangaroo rat
mounds. Individual kangaroo rats continually remodeled mounds in
response to seasonal conditions. Compared to summer, mounds in winter had approximately 50% fewer entrances and plugged entrances were
common. Monthly differences in number of entrances were closely
linked with seasonal changes in soil temperature and precipitation.
Number of entrances decreased as soil temperature and precipitation
declined. Changes in burrow entrances likely reflect seasonal differences
in the relative importance of burrow functions. Fewer burrow entrances
during winter would create a warmer microclimate by reducing convective heat loss in mounds, resulting in thermoregulatory savings for occupants. During the summer, thermoregulatory costs of kangaroo rats are
low, but risk of seed cache spoilage and predation from snakes increases.
Adding burrow entrances after large summer rainfall events would
increase the evaporation rate within mounds, reducing spoilage of seed
caches. More burrow entrances would also reduce predation risk in the
summer by providing additional escape routes.
Introduction
Burrows serve many functions for animals by providing a location for rearing young, sleeping, hibernation, food storage, and protection from predators
and environmental extremes (Reichman & Smith
1990; Kinlaw 1999). Architectural features of burrows such as depth, orientation, and number of
entrances can enhance specific functions critical to
the occupant’s fitness. In particular, burrow architecture across many taxa and habitats plays a major
role in thermoregulation (Korb & Linsenmair 1998,
2000; Kleineidam et al. 2001; Bulova 2002). The soil
surrounding burrows creates a buffering effect,
which shields occupants from diurnal fluctuations in
430
surface temperature and humidity (Burda et al.
2007). Depth and ventilation affect the degree of
buffering from surface conditions and can be adjusted by occupants to create microclimates closer to
optimum conditions (Roper & Kemenes 1997;
Bulova 2002; Shimmin et al. 2002; Roper & Moore
2003). As a result, semi-fossorial animals can avoid
physiologically stressful surface conditions by taking
refuge in burrows (King 1980; Reichman & Smith
1990; Prakash 1997; Kinlaw 1999).
Animals may also configure burrows to reduce
predation risk. Both comparative and experimental
studies indicate that semi-fossorial rodents in habitats with high predation risk have greater numbers
of burrow entrances, which likely aid in escape
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
Seasonal Changes in Burrow Architecture
A. J. Edelman
(Harper & Batzli 1996; Jackson 2000). In addition,
many semi-fossorial animals rely on cached food to
survive through prolonged periods of scarcity. Burrow architecture can be altered to provide suitable
microclimates for food preservation, reducing cache
losses from decomposers (Reichman & Smith 1990;
Vander Wall 1990). Seasonal changes in climate,
predation risk, and caching behavior suggest that
occupants may respond by modifying burrow architecture. However, evidence of seasonal modification
is limited to anecdotal observations of plugged burrows during thermally stressful conditions (Luckenbach 1982; Kawamichi 1989; Arnold et al. 1991) or
use of burrows at different depths during summer
and winter (Bartholomew & Hudson 1961; Ghobrial
& Hodieb 1973; Scheibler et al. 2006).
Kangaroo rats (Dipodomys spp.) are a model organism for observing burrow modification in response
to seasonal changes because their burrow environment, physiology, and behavior have been well
documented (Genoways & Brown 1993). These nocturnal, non-hibernating rodents are native to semiarid ecosystems of western North America (Holdenried 1957; Kenagy 1973; Kay & Whitford 1978;
French 1993; Schmidly et al. 1993). One of the largest and most behaviorally complex species in this
genus is the banner-tailed kangaroo rat (Dipodomys
spectabilis), which inhabits grassland and shrub lands
of the southwestern United States and northern
Mexico (Best 1988; Jones 1993). This solitary species
constructs and aggressively defends mounds containing an elaborate burrow system (Schroder 1979).
Mounds are typically 4 m in diameter and 30 cm in
height with multiple entrances (Fig. 1) (Holdenried
(a) Winter
1957; Reichman et al. 1985). The burrow system is a
labyrinth of tunnels and chambers extending up to
four levels and >90 cm in depth (Vorhies & Taylor
1922). New mounds are rarely built in established
populations. Instead offspring disperse to unoccupied
mounds or inherit the natal mound (Jones 1984).
Mounds provide thermal refugia for kangaroo rats
from extreme surface temperatures that range from
near 40C during summer to below freezing during
the winter (Kay & Whitford 1978). Thermoregulatory costs for kangaroo rats are generally highest
during the winter, when ambient temperature drops
below thermoneutrality (Carpenter 1966; Kenagy
1973; Hinds & MacMillen 1985).
Within mounds, banner-tailed kangaroo rats larder
hoard up to 5 kg of collected seeds to survive periods
of resource scarcity (Vorhies & Taylor 1922). Caching occurs most frequently during spring and
autumn, when seed availability is highest (Vorhies &
Taylor 1922; Monson 1943). Maintaining a low-tomoderate moisture microclimate within mounds is
critical to seed preservation because high-moisture
conditions (e.g. after large rainfall event) lead to
cache loss because of germination and toxic fungal
infections (Hawbecker 1940; Reichman et al. 1985;
Frank 1988; Valone et al. 1995).
A variety of terrestrial and aerial vertebrates prey
on banner-tailed kangaroo rats, and annual adult
survivorship is low (<50%) (Vorhies & Taylor 1922;
Nader 1978; Waser & Jones 1991). Predation risk
also varies seasonally because snakes are dormant
during the colder half of the year. Snakes are one of
the few predators that enter mounds in pursuit of
kangaroo rats (Randall & Stevens 1987).
(b) Summer
Fig. 1: Typical banner-tailed kangaroo rat mounds during winter (a) and summer (b) with visible burrow entrances marked with white arrows.
Note the greater number of burrow entrances in summer compared to winter. For scale, the child in the picture is approximately 1-m tall.
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
431
Seasonal Changes in Burrow Architecture
My objective was to examine how banner-tailed
kangaroo rats modify burrow architecture in
response to seasonal changes in thermoregulatory
costs, predation risk, and vulnerability of caches to
spoilage. Over 3 yr, I monitored the relationship
between number of burrow entrances in mounds
and climate in a northern Chihuahuan Desert population of banner-tailed kangaroo rats. During the
winter, thermoregulatory costs for kangaroo rats are
high, whereas predation risk is lower because of dormancy of predatory snakes. Spoilage of seed caches
is also lower at this time because of drier and colder
conditions, which inhibit seed germination and fungal growth. Conversely, during the summer when
rainfall and temperatures are greater, thermoregulatory costs are lower and risk of predation and cache
spoilage are higher. I predict that kangaroo rats will
reduce the number of burrow entrances in mounds
during winter (Fig. 1a) and increase them during
summer (Fig. 1b) in response to these changes. More
entrances during summer would aid in escape from
predators and speed evaporation after rainfall events,
whereas fewer entrances during winter would
reduce incursion of cold air resulting in lower thermoregulatory costs.
Materials and Methods
Study Area
The study area was located at the Sevilleta National
Wildlife Refuge, near Socorro, New Mexico, USA
(3424¢24.8¢N, 10636¢20.5¢W, 1600 m elevation).
The site encompassed 18 ha of Chihuahuan Desert
and short grass steppe vegetation dominated by
grama grass (Bouteloua eriopoda and B. gracilis), burrograss (Scleropogon brevifolius), and sand dropseed grass
(Sporobolus cryptandrus). Soil was classified as deep
clayey loam.
Mound Census
The study area contained 165 kangaroo rat mounds
of varying condition and size. Each mound was
mapped and uniquely marked. From Mar. 2005 to
Feb. 2008, I performed a monthly census of the banner-tailed kangaroo rat population on the study
area. Each month (excluding Mar., April, and June
2006 and Jan. 2007), all mounds were assessed for
signs of kangaroo rat activity (e.g. fresh digging and
feces, burrow entrances free of debris) (Jones 1984).
At each mound, I counted the number of opened
and plugged burrow entrances approximately ‡5 cm
432
A. J. Edelman
in diameter. This criterion was based on the minimum size entrance I observed kangaroo rats to
enter. It is unlikely that other species created substantial numbers of entrances into occupied mounds.
Other rodent species avoid mound areas probably
because of the aggressive nature of banner-tailed
kangaroo rats and reduced vegetation cover (Frye
1983; Bowers & Brown 1992). Kangaroo rats also
quickly repair unauthorized openings into mounds
(personal observation). A plugged burrow entrance
was a soil-filled area on the mound, which retained
the visible outline of the former opening. Bannertailed kangaroo rats on my study area did not plug
entrances during the day as reported in more southerly populations (Randall & Stevens 1987). Thus,
any changes in burrow entrances between months
were considered semi-permanent. Kangaroo rats
often covered plugged entrances completely with soil,
making them difficult to detect. Therefore, I used the
presence or absence of plugged entrances on mounds
in analyses, rather than the total number.
All mounds exhibiting active kangaroo rat signs
were trapped for three consecutive nights each
month. Two to four live traps (Model XLK, H.B.
Sherman Traps, Tallahassee, FL, USA) were baited
with sweet feed (oats, corn, and barley mixed with
molasses) and placed at each mound (Cross & Waser
2000). I opened live traps at dusk and examined
them 3–7 h after sunset. All individuals were marked
with a uniquely numbered passive integrated transponder tag (Model 1440ST; Biomark, Boise, ID, USA),
which was injected subcutaneously. I recorded
gender, age, reproductive status, and mass of all captured individuals. An individual captured most frequently at a mound could reliably be considered the
occupant (Schroder 1979; Jones 1984; Waser et al.
2006). During this study, I considered a mound
occupied by an individual if it was caught at the
mound >1 month and more frequently than any
other adult. All animals were handled under methods approved by the University of New Mexico Institutional Animal Care and Use Committee (Protocol
No. 04MCC00507 and UNM048-TR-100261).
Data Analysis
All statistical analyses were conducted using R
version 2.10.0 (R Development Core Team 2009).
Precipitation and mean, minimum, and maximum
air and soil temperature at 10 cm were recorded
hourly by a data logger (Model CR10X; Campbell
Scientific Inc., Logan, UT, USA) located 6.6 km
from the study area in grassland habitat (1650 m
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
Seasonal Changes in Burrow Architecture
A. J. Edelman
elevation). Mean soil temperature at 10 cm has been
shown to closely match mean burrow air temperature at depths <30 cm in banner-tailed kangaroo rat
mounds (Kay & Whitford 1978). Hourly readings for
mean temperature data were averaged, and maximum and minimum temperatures were determined
for each day. For each month, I calculated a time
series dataset containing mean daily air temperature
and soil temperature at 10 cm (minimum, mean,
and maximum), total precipitation, and mean number of burrow entrances (based on all occupied
mounds).
Data in the time series exhibited significant autocorrelation between consecutive months. Therefore,
I used generalized least squares (GLS) regression
with autocorrelated errors to examine whether
long-term trends in climate variables existed and
how mean number of burrow entrances varied in
response to possible explanatory variables. Autocorrelated errors (q) were modeled in GLS regression
as a first-order autoregressive process, preventing
underestimation of standard errors and inflated
p-values for effects in regression models (Venables &
Ripley 2002; Cowpertwait & Metcalfe 2009). The
extended length of the dataset (32 months) provided
enough statistical power to accurately estimate autocorrelation (Swanson 1998). I tested for long-term
trends (e.g. increasing temperature) individually for
each climate variable by comparing the fit of GLS
models with (full model) and without a long-term
trend component (null model) using a likelihood
ratio test. Both the full and null models contained a
harmonic seasonal component that allowed climate
variables to change seasonally (Cowpertwait &
Metcalfe 2009; Crawley 2009). I used GLS regression
to determine how mean burrow entrance number
varied in response to possible explanatory variables
including mean soil temperature at 10 cm, mean air
temperature, total precipitation, interactions among
climate variables, and time.
I examined how individual kangaroo rats changed
the number of burrow entrances in their mounds
between July and Dec. by fitting a linear mixed
model. These months were selected because they
represented seasonal differences between summer
and winter, and census data were available for all
years. Fixed effects in the full model were sex, year
(2005, 2006, and 2007), month (July and Dec.), and
interactions between effects. Identity of kangaroo
rats was included as a random effect on the intercept
to control for pseudoreplication from multiple observations on the same individuals. Only mounds that
were occupied by the same individual during July
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
and Dec. of the same year were included in the
model. The count-based-dependent variable, number
of entrances, was square-root transformed to normalize the distribution.
GLS regression and linear mixed models were fitted using the maximum likelihood method for use
in likelihood ratio tests and the variable selection
process; final models were fitted using the less-biased
restricted maximum likelihood (REML) method.
Effects included in final models were chosen
through backwards selection. Beginning with the full
model, the least significant effects were sequentially
removed, and the nested models were compared
using a likelihood ratio test (Zuur et al. 2009). I used
a Pearson chi-square test with Yates’ continuity correction to compare proportion of mounds with and
without plugged burrow entrances between July and
Dec. All data met the assumptions of parametric tests
and only two-tailed p-values were reported. I considered p values < 0.05 significant.
Results
Climate variables exhibited strong seasonal patterns,
but no long-term trends (e.g. decreasing or increasing temperature) over the duration of the study
(Fig. 2). For total precipitation and mean daily minimum, mean, and maximum temperatures of surface
air and soil at 10 cm, GLS regression models containing only a harmonic seasonal component were a
better fit (likelihood ratio tests, all p > 0.65) than
models with a long-term trend component also
included.
Mean number of burrow entrances in occupied
mounds exhibited a strong seasonal pattern, varying
from a high of 10–12 during the summer to a low of
4–6 during winter depending on the year (Fig. 2).
The number of occupied mounds each month ranged from 35 (1.9 mounds ⁄ ha) in Mar. 2005 to 103
(5.7 mounds ⁄ ha) in Aug. and Sept. 2005 (x SE =
62.6 3.3 mounds). Monthly fluctuations in mean
number of burrow entrances closely matched
changes in soil temperature at 10 cm (Fig. 2a) and
air temperature (Fig. 2b). The peaks in number of
burrow entrances each year corresponded to months
when total precipitation exceeded 60 mm (Fig. 2c).
The best-fitting GLS regression model included mean
soil temperature at 10 cm and total precipitation as
explanatory variables of mean number of burrow
entrances each month (Table 1; residual standard
error = 1.32). During the variable selection process,
mean air temperature and interactions were not significant effects. After fitting the reduced model using
433
Seasonal Changes in Burrow Architecture
40
A. J. Edelman
Soil temperature at 10 cm
Table 1: Best-fitting generalized least squares regression model with
autocorrelated errors (q) for the mean number of burrow entrances in
occupied banner-tailed kangaroo rat mounds from Mar. 2005 to Feb.
2008
14
(a)
Temperature (°C)
10
8
20
6
4
10
Burrow entrances
12
30
Effects
Estimate
SE
t29
p
Intercept
Soil temperature at 10 cm
Precipitation
q
4.55
0.15
0.015
0.72
0.71
0.03
0.006
6.4
5.4
2.6
<0.0001
<0.0001
0.014
2
0
0
Air temperature
14
(b)
Temperature (°C)
10
20
8
6
10
4
0
2
0
–10
120
Precipitation
14
(c)
12
100
Precipitation (mm)
Burrow entrances
12
30
10
80
8
60
6
40
4
20
Burrow entrances
40
2
0
0
Jul
2005
Jan
2006
Jul
2006
Jan
2007
Jul
2007
Jan
2008
Fig. 2: Relationship between mean number of burrow entrances
(solid line) in occupied banner-tailed kangaroo rat mounds and mean
soil temperature at 10 cm (a), mean surface air temperature (b), and
total precipitation (c) each month from Mar. 2005 to Feb. 2008. Precipitation and mean daily temperatures are represented by dashed
lines and mean daily minimum and maximum temperatures by dotted
lines. Predicted mean burrow air temperature each month (dotted and
dashed line in b) was calculated from mean daily surface air temperature based on a linear equation of the observed relationship between
surface air temperature (TA) and burrow air temperature (TB):
TB = )2.12 + 0.88TA. The equation was derived from measurements at
a variety of depths (10–90 cm) in kangaroo rat mounds and should be
interpreted as an average predicted TB of the mound (Kay & Whitford
1978).
434
the less-biased REML method, time became a nonsignificant effect and was removed from the final
model. Mean number of burrow entrances in occupied mounds decreased with mean soil temperature
at 10 cm and increased with precipitation. For each
6.7C (95% CI = 4.8–11.1C) decrease in mean soil
temperature, number of burrow entrances are predicted to decrease by an average of approximately 1,
whereas 67 mm (95% CI = 39–333 mm) of precipitation results in a predicted mean increase of 1 burrow entrance.
Individual kangaroo rats actively remodeled their
mounds between seasons. In the best-fitting linear
mixed model (Table 2; based on 236 observations of
89 individuals), entrance number decreased on
mounds from July to Dec. after controlling for effects
of sex and year. The change between seasons in
entrance number was more pronounced for females
than males as indicated by the significant interaction
between sex and month (all other interactions were
not significant). Mounds of females (n = 61) had
more entrances during July than those of males
(n = 57), but entrance numbers were similar between sexes during the winter (Fig. 3). Based on the
significant effect of year, the number of entrances
on mounds also moderately increased each year of
Table 2: Best-fitting linear mixed model for the square-root transformed number of burrow entrances in mounds of individual bannertailed kangaroo rats during July and Dec. from 2005 to 2007
Effects
Estimate
SE
t
df
p
Intercept
Sex: male
Month: July
Year: 2006
Year: 2007
Sex: male · Month: July
2.09
)0.01
1.08
0.25
0.41
)0.25
0.10
0.13
0.08
0.10
0.09
0.11
20.6
)0.1
13.7
2.7
4.4
)2.2
143
87
143
143
143
143
<0.0001
0.94
<0.0001
0.008
<0.0001
0.030
The intercept represents the predicted value for females during Dec.
2005. A random effect on the intercept for the identity of the kangaroo rat was included in the model (SD = 0.45; residual SD = 0.43).
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
Seasonal Changes in Burrow Architecture
A. J. Edelman
14
2.0
2.0
1.5
1.5
1.0
1.0
0.5
0.5
8
6
4
2
mg H2 O/g h
10
ml O2 /g h
Burrow entrances
12
0
July
December
0.0
0.0
0
Fig. 3: Number of burrow entrances (x SE) at mounds of female
(white bars) and male (gray bars) banner-tailed kangaroo rats during
July and Dec. from 2005 to 2007.
the study (2005: x SE = 7.4 0.4; 2006:
x SE = 8.1 0.5; 2007: x SE = 9.4 0.5). Total
numbers of mounds occupied by the same kangaroo
rat during both July and Dec. on site were 47 in
2005, 28 in 2006, and 43 in 2007. Plugged burrow
entrances at mounds occupied by the same individuals were almost never detected in July (2%, 2 of 118
mounds) and were more commonly found in Dec.
(35%, 41 of 118 mounds) for all years combined
(n = 236, v21 = 41.1, p < 0.0001).
Discussion
Banner-tailed kangaroo rats seasonally remodeled
mounds. These surface alterations in mound architecture closely mirrored changes in soil temperature
and precipitation (Fig. 2). Decreases in burrow
entrances were tightly linked with drops in soil temperature at 10 cm and periods of low precipitation.
Compared to summer when soil temperatures and
precipitation were higher, mounds in winter averaged half as many openings (Fig. 1). Modifications of
burrows were intentional, because mounds occupied
by the same kangaroo rat differed in number of
entrances between winter and summer (Fig. 3).
Changes in burrow architecture were likely adaptive
responses by kangaroo rats to seasonal changes in
thermoregulatory costs, predation risk, and seed
spoilage.
Fewer entrances in winter reduce heat loss from
air convection and increase soil-buffering effects creating a more stable and warmer microclimate within
burrows (Roper & Kemenes 1997; Bulova 2002;
Shimmin et al. 2002; Roper & Moore 2003). At cold
surface temperatures, warm air in burrows convectively rises and escapes aboveground and colder air
from the surface sinks into burrows, reducing the
buffering effect of the surrounding soil (Nikol’skii &
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
10
20
30
Ambient temperature (°C)
40
Fig. 4: Predicted mass-specific basal metabolic rate (BMR; solid line
with circles) and evaporative water loss (EWL; dashed line with triangles) of banner-tailed kangaroo rats at different ambient temperatures. Predictions were calculated from allometric equations of
desert heteromyid rodents (Hinds & MacMillen 1985) based on a
body mass of 141.4 g (mean adult mass). Predicted BMR was calculated at 5C, 15C, and thermoneutrality (25–35C) using the following equations: BMR5 ¼ 27:938M 0:571 , BMR15 ¼ 15:720M 0:508 , and
BMRTN = 2.993M)0.271, where M is body mass. Predicted BMR at 0C
was estimated through linear regression of BMR at higher temperatures.
Predicted EWL was calculated at 5–25 and 35C using the following
equations: EWL525 ¼ 5:267M 0:368 and EWL35 ¼ 4:711M 0:211 .
Savchenko 2002). Thus, kangaroo rats can reduce
incursion of cold air into burrows by sealing
entrances during the winter months. To better
understand how changes in burrow temperature
could affect important metabolic processes, I used
published allometric equations to predict mean burrow air temperatures (Fig. 2b; dotted and dashed
line), basal metabolic rate (BMR), and evaporative
water loss (EWL; Fig. 4) for banner-tailed kangaroo
rats in my study (Kay & Whitford 1978; Hinds &
MacMillen 1985). Winter burrow air temperatures
in banner-tailed kangaroo rat mounds at lower elevation sites in southern New Mexico averaged
5–10C (Kay & Whitford 1978; French 1993). Predicted burrow air temperatures at my higher elevation and latitude site were even lower ranging from
)2 to 1C during Dec. and Jan. (Fig. 2b) which are
below the lower limit of thermoneutrality by
approximately 25C. At these temperatures, predicted BMR of banner-tailed kangaroo rats was
approximately two and half times higher than at
thermoneutrality (Fig. 4), likely resulting in increased food consumption for thermoregulation (Hinds
& MacMillen 1985). While banner-tailed kangaroo
rats use an insulated nest chamber to reduce exposure to cold burrow air temperatures, they remain
active all year even under inclement weather
(Vorhies & Taylor 1922; Schroder 1979). The lack of
seasonal differences in activity levels, probably
435
Seasonal Changes in Burrow Architecture
because of the year-round necessity of territorial
defense and management of seed caches (French
1993), increases banner-tailed kangaroo rats’ exposure to cold temperatures. Remodeling burrows to
improve soil-buffering effects would result in significant energy savings through lower BMR and
decrease the rate at which seed caches were
depleted. For example, maintaining burrow air temperatures at 5C warmer than minimum surface air
temperatures during the winter would reduce BMR
by approximately 15% (Fig. 4).
During the summer, thermoregulatory costs of
kangaroo rats are relatively lower than the winter,
but predicted EWL can increase if temperatures are
above 25C (Fig. 4). Burrow air temperatures of banner-tailed kangaroo rats at lower elevations were
between 25 and 30C, within the thermoneutral
zone (Kay & Whitford 1978). At my site, predicted
burrow air temperatures were lower, ranging from
20 to 22C during June and July (Fig. 2b). While
these mean temperatures are slightly below thermoneutrality, soil temperatures at 10 cm indicated that
air temperature in burrows at depths <30 cm would
be within 29–33C (Fig. 2a). Given this range of
temperatures, banner-tailed kangaroo rats should be
able to move vertically within the burrow system to
seek temperatures that minimize both BMR and
EWL, as observed in other kangaroo rat species
(Kenagy 1973).
More burrow entrances on mounds at warm temperatures may be a strategy by kangaroo rats to
reduce predation risk, which is greater during warmer periods when snakes are active. From approximately Oct. to early April, large snakes such as the
Western diamondback rattlesnake (Crotalus atrox) are
dormant on my study site, and only mammalian and
avian predators are active (personal observation).
More burrow entrances during the summer may
decrease predation success by providing additional
escape routes while kangaroo rats are either aboveground or belowground (Bronner 1992). Other
rodent species also exhibit increased number of
entrances when at higher predation risk. In whistling rats (Parotomys spp.), species in habitats with
higher predation risk had more burrow entrances
than species in habitats with lower predation risk
(Jackson 2000). Voles (Microtus spp.) in pens with
predators (including snakes) built more complex
burrows with additional entrances than in pens
without predators, suggesting that these modifications reduce predation risk (Harper & Batzli 1996).
Kangaroo rats likely attempted to reduce germination and extreme fungal growth in seed caches dur436
A. J. Edelman
ing wet periods by increasing ventilation within
mounds via more entrances. Peaks in number of
burrow entrances corresponded closely with months
of high precipitation (>60 mm) on the study site
(Fig. 2c). High levels of fungal infections in seed
caches occur within mounds after rainfall (Reichman et al. 1985). While banner-tailed kangaroo rats
may prefer slightly moldy seeds, they avoid eating
very moldy seeds and actively manage seed caches
to reduce major fungal infections (Reichman &
Rebar 1985; Reichman et al. 1986; Frank 1988; Herrera et al. 2001). Massive fungal contamination of
seed caches with mycotoxins are implicated in the
near-extirpation of banner-tailed kangaroo rats following a large rainfall event of 129 mm in Arizona
(Valone et al. 1995), indicating that significant cache
loss can greatly impact fitness. More entrances during periods of high precipitation would increase passive ventilation of mounds, lower humidity, and
speed evaporation of water from saturated burrows
and caches (Schmidt-Nielsen & Schmidt-Nielsen
1950; Vogel & Bretz 1972; Vogel et al. 1973). Banner-tailed kangaroo rat mounds are well ventilated
during the summer; relative humidity in burrow air
is typically around 30%, substantially lower than
100% relative humidity found in plugged underground air spaces (Schmidt-Nielsen & Schmidt-Nielsen 1950).
Besides the strong seasonal pattern of remodeling,
minor differences in mound modification were detected between sexes and among years. The greater
number of entrances at mounds of females during
the summer may be attributable to the presence of
dependent offspring. Females typically give birth to
1–3 offspring during late winter and early spring.
Offspring remain at their mother’s mound until
approximately 3-5 months of age and in some cases
even longer (Waser et al. 2006; Edelman 2010). Offspring may have contributed to more entrances at
females’ mounds compared to males’ during the
summer through additional burrowing activity or as
the result of increased predation risk because of the
higher densities of kangaroo rats at these locations.
The moderate increase in the number of entrances
over each year of the study was not driven by
changes in climate, because there were no long-term
trends for increasing summer temperatures or precipitation during the study. Other factors such as
changes in predation risk, identity of occupied
mounds (e.g. age and size), or observer bias (e.g.
improvement in burrow entrance identification over
time) may have contributed to the observed increase
during the study.
Ethology 117 (2011) 430–439 ª 2011 Blackwell Verlag GmbH
A. J. Edelman
There is little existing quantitative evidence on how
non-hibernating, semi-fossorial mammals modify
burrows in response to seasonal changes in environmental conditions. This is likely due to absence of
long-term monitoring of burrow systems. Most
detailed studies of burrow architecture are necessarily
destructive, eliminating the possibility of comparisons
between seasons. Monitoring surface architecture of
burrows is a non-destructive technique, which can
provide insight into an animal’s reaction to changes
in climate, predation risk, and other environmental
conditions. Kangaroo rats are well known for their
physiological and morphological adaptations to arid
environments (Brylski 1993; French 1993). My
results highlight how behavioral adaptations are also
critical to their success at surviving in arid habitats.
Acknowledgements
I thank S. Collins, J. Edelman, M. Friggens, J. Johnson, V. Mathis, D. Moore, L. Schwanz, B. Wolf, and
numerous undergraduate students for technical and
field assistance with this study. I thank A. KodricBrown, J. Brown, G. Roemer, F. Smith, and two
anonymous reviewers for insightful comments on
this manuscript. This research was funded by the
Sevilleta Long Term Ecological Research Site Graduate Student Summer Grant, American Society of
Mammalogists Shadle Fellowship and Grant-in-Aid,
Southwestern Association of Naturalists Howard
McCarley Student Research Award, T & E, Inc.
Grant for Conservation Biology Research, and the
University of New Mexico Gaudin Scholarship in
Mammalogy, Grove Summer Scholarship, Student
Research Allocation Committee Research Grant,
Biology Graduate Student Organization Research
Grant, and Graduate Research Development Fund. I
received financial support from a National Science
Foundation Teaching Fellowship in K–12 Education
and the University of New Mexico Biocomplexity
and Regents’ Graduate Fellowships.
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