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. Literature Cited Arnold, W., Heldmaier, G., Ortmann, S., Pohl, H., Ruf, T. & Steinlechner, S. 1991: Ambient temperatures in hibernacula and their energetic consequences for alpine marmots (Marmota marmota). J. Therm. Biol. 16, 223—226. Bartholomew, G. 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