The energy cost of voluntary running in the weasel Mustela nivalis

The small weasels in the genus Mustela have one of the more unusual morphologies among terrestrial mammals, characterized by very elongate bodies, narrow heads, long necks and short legs. This body form is presumed to have evolved to facilitate movement within the burrows of rodents, which are the principal prey of weasels (King, 1983; King, 1989; Jedrzejewska and Jedrzejewski, 1998). This ability to maneuver within confined tunnels is probably a key factor in the ecological success of weasels, which have a very wide Holarctic distribution and occupy a diverse range of habitats including deserts, grasslands, tundra and forests. However, it also has costs. Coupled with fairly short pelage and an inability to store substantial subcutaneous fat deposits, the elongate shape of weasels is thought to be a causal factor in their exceptionally high basal metabolism and thermal conductance (Scholander et al., 1950; Iversen, 1972; Brown and Lasiewski, 1972; Moors, 1977; Casey and Casey, 1979; Szafrañska et al., 2007). Inclusion of these traits into biophysical models suggests that weasels are seldom active in themoneutral conditions in many parts of their extensive Holarctic range (Chappell, 1980), and recent doubly labeled water studies (Zub et al., 2009) show that the daily energy expenditures (DEE) of weasels are higher than allometric predictions for carnivores (Nagy et al., 1999).

In the context of ecology and energetics, another possible repercussion of weasel body form is the metabolic cost of locomotion. Although their shape seems adapted to moving within burrows, weasels are often active elsewhere in their habitats and, at least in some circumstances, may travel over substantial distances (King, 1989; Jedrzejewski et al., 2000). The morphology of weasels is strikingly different from the compact body form and long, thin legs of ‘classic’ cursorial species such as canids, horses, deer and antelope (e.g. Alexander, 2003). Given that contrast in shape, a reasonable inference is that the short legs and elongate bodies of weasels could result in a high energetic cost of terrestrial movement. Results from several studies suggest that elongate mustelids do have higher than predicted transport costs, but all are from animals considerably larger than weasels and two of the tested species were semi-aquatic (Taylor et al., 1982; Williams, 1983; Williams et al., 2002).

More broadly, the importance of locomotor costs as a component of DEE in small mammals is controversial. Estimates of the ‘ecological cost of transport’ for daily movement distances derived from home range size suggested that the fraction of DEE used to power locomotor exercise is quite minor in most small mammals, but could comprise a substantial portion of the daily energy budget of carnivores with large home ranges (Garland, 1983). In contrast, studies of movement distances, running behavior and exercise metabolism of rodents in natural habitats (e.g. Kenagy and Hoyt, 1989), or of voluntary running of small mammals in captivity (e.g. Koteja et al., 1999; Chappell et al., 2004; Chappell and Dlugosz, 2009), suggest that movement costs could comprise 5–20% of DEE. The importance of locomotor expenditures in the DEE of weasels is of interest because they are both small and carnivorous (Mustela nivalis is the smallest member of the order Carnivora) and seem to show a seasonal trade-off between activity and thermoregulation, which is consistent with a relatively high cost of activity (Zub et al., 2009).

In this study we examined several aspects of running performance and energetics in weasels. We performed laboratory measurements of energy metabolism during voluntary locomotor exercise to obtain the energy cost of transport in semi-natural conditions. We also determined maximal oxygen consumption in forced exercise for comparison with voluntarily attained exercise intensity. We took advatage of the unusually large fourfold range in weasels’ adult body mass (King, 1989; Zub et al., 2009) to examine intraspecific metabolic scaling and its effect on energy expenditures. Finally, we combined the laboratory measurements with radiotracking studies of movements and previously reported doubly labeled water measurements of DEE to estimate the importance of locomotor costs in weasel energy budgets in natural habitats.

We worked with a well-studied population of weasels (Mustela nivalis Linnaeus 1766) in the Białowieza Forest region in northeastern Poland, including the Białowieza Glade and Białowieza National Park (23.86°E, 52.70°N). Local habitats included old-growth hardwood forest, agricultural fields and meadows, and in riparian areas, sedge meadows, wet grassy meadows and reedbeds. Weasels were captured in wooden box-traps (Jedrzejewski et al., 1995) under the auspices of Polish nature conservancy authorities (permits DOPweg-4201-04-6/03/jr, DOPog-4201-04-43/05/aj, LKE 2003/04 and LKE 2004/06).

Previous work on this weasel population has included measurements of activity patterns (Jedrzejewski et al., 1995; Jedrzejewski et al., 2000), resting energy metabolism (Szafrañska et al., 2007), habitat use (Jedrzejewski and Jedrzejewski, 1998; Zub et al., 2008) and field metabolic rates (Zub et al., 2009), and we followed the handling procedures detailed in those studies. In brief, captured weasels were transported to our laboratory at the Mammal Research Institute in the town of Białowieza, housed in cages that included a shelter with bedding, and provided with water ad libitum and one to two laboratory mice per day (depending on weasel body mass). Animals were released the day after all measurements were completed. All procedures complied with the Principles of Animal Care (publication no. 86-23, revised 1985) of the US National Institutes of Health and were approved by the Institutional Animal Care and Use Committee of the University of California, Riverside, and the Local Research Ethics Committee in Białystok (permits LKE 2003/04, LKE 2004/06, LKE 2005/08, LKE 8/2006 and LKE 42/2008).

Weasels used for radiotracking studies were fitted with a neck-collar radio transmitter under ketamine-xylazine anesthesia (Jedrzejewski et al., 2000). Collared animals were released at the site of capture and their position and activity were checked every 15–60 min throughout the period of daylight [weasels in the Białowieża region are rarely active at night (Jedrzejewski et al., 2000)]. Bearings were taken from a distance of at least 50 m to avoid disturbance by the observer. These studies were carried out in June through November in 1997–2006, and included 35 animals tracked. In analyses we used data collected over one to four consecutive days of radiotracking.

We measured energy costs as rates of oxygen consumption (V̇_O2) using open-circuit respirometry, with a conversion factor of 20.1 J ml^–1 O₂. Outside air was pumped into the metabolic system under positive pressure. Incurrent air was dried with Drierite (Hammond, Xenia, OH, USA) and metered (±1%) with ERG-1000 mass flow controllers (Warsaw, Poland) before entering the metabolic chambers. Excurrent air from the chambers was subsampled with an SS-3 pump (Sable Systems, Las Vegas, NV, USA), dried and flowed through a Sable Systems FC-1b oxygen analyzer. Instrument outputs were digitized with a Sable Systems UI2 and recorded with a Macintosh Powerbook running LabHelper software (www.warthog.ucr.edu).

Most of the metabolic tests were performed on weasels captured in September and October 2007, with a few animals tested in June and July 2008.

We measured maximum rates of oxygen consumption (V̇_O2,max) during forced exercise in an enclosed running wheel constructed of plexiglass. The wheel had a circumference of 0.69 m and an internal volume of 3.0 l. The running surface was lined with friction tape for traction. Air entered and exited through airtight axial bearings equipped with manifolds to disperse flow and increase mixing, which was also facilitated by wheel rotation and by movements of the animals. Flow rates were 2000 ml min^–1 STP. Subsampled excurrent air (∼150 ml min^–1) was scrubbed of CO₂ with soda lime and dried prior to oxygen analysis. Flow rate and O₂ content were recorded every 1 s.

We used a larger enclosed running wheel respirometer to measure energy costs and behavior during voluntary running and resting. The chamber [fig. 1 in Chappell et al. (Chappell et al., 2004)] was constructed of plexiglass and contained a standard polycarbonate mouse cage as well as a 1.12 m circumference stainless steel and plexiglass running wheel (Lafayette Instruments, Lafayette, IN, USA). Bedding and a drinking tube were available in the mouse cage, which was connected to the wheel through a short 7.7 cm diameter tunnel. Flow rate was 2500 ml min^–1 STP, and a small fan circulated air within the chamber to improve mixing. A tachometer transduced the speed and direction of wheel rotation. A computer-driven multiplexer (Sable Systems TR-1) obtained a reference reading of unbreathed air for 2.5 min every 45 or 60 min. Wheel motion, flow rate and O₂ concentration were recorded every 1.5 s. Weasels were left in the wheel chambers for 8–24 h and were given food (laboratory mice) when kept in wheels for more than 10 h. Tests were run at the ambient photoperiod (the laboratory was illuminated through windows) and temperature (17–24°C). As during V̇_O2,max tests, weasels running voluntarily remained near the bottom of the wheel, with little tendency to run ‘uphill’ or ‘downhill’.

We computed minimal resting metabolic rate (RMR_min) as the lowest 10 min continuous mean of V̇_O2 during periods when animals were inactive (as indicated by low and stable V̇_O2). Maximal voluntary V̇_O2 was calculated as the highest 1, 2 and 5 min continuous means of V̇_O2 when animals were running in the wheel. We also determined the total distance run and time spent running, the maximum instantaneous speed (i.e. the highest speed in a 1.5 s interval), the highest 1, 2 and 5 min continuous means of speed, and the mean speed (total distance run/total time spent running).

To obtain the relationship between running speed and V̇_O2 we used the LabAnalyst stepped-sampling procedure to compute 1 min sample means of speed and V̇_O2, with successive 1 min samples separated by 3 min to avoid autocorrelation problems (Chappell et al., 2004; Rezende et al., 2005; Rezende et al., 2006). Samples with mean speed <0.03 km h^–1 were discarded (data from speeds this low were inaccurate due to background electrical noise in the tachometer). We also discarded data from weasels that did not run faster than 0.9 km h^–1. For the remaining animals, we regressed the 1 min means of speed and V̇_O2 to obtain slopes and intercepts.

Regressions of speed and V̇_O2 can be used to calculate costs of transport (COT; energy used to move a unit mass a given distance; i.e. kJ kg^–1 km^–1). To convert O₂ consumption to energy, we assumed 20.1 J ml^–1 O₂. Absolute COT at a given speed is computed as power/speed; this typically decreases as speed increases because the speed versus power regression has a non-zero (positive) intercept. A speed-independent measure of transport costs is the ‘incremental’ COT (iCOT), which is the slope of the speed versus power regression.

The stepped-sampling procedure is not readily applicable for short bouts of wheel activity, and most weasels did not run for extended periods (Fig. 1). Accordingly, we used a second approach to estimate costs of transport in a larger number of individuals. When bouts of wheel-running occurred in the absence of other activity (as determined from V̇_O2), we integrated each bout’s running speed data (to obtain total distance traveled in km) and V̇_O2 (to obtain total ml O₂ consumed). We also measured bout duration and the resting metabolic rate (RMR, ml O₂ min^–1) immediately before or after the bout. Mean speed was computed as total distance/bout duration, and net O₂ consumption due to running was computed as: total O₂ consumption–(RMR×bout duration). Cost of transport (kJ km^–1) at the mean speed was calculated as net O₂ consumption/total distance, using a conversion factor of 20.1 J ml^–1 O₂.

Because there was a wide body mass range in our animals and metabolic rates are a power function of mass, we log₁₀-transformed mass and metabolism prior to analyses. We used ANOVA, ANCOVA and simple and multiple least-squares regression models for most analyses. A linear mixed model with animal ID as a random variable was used in analyses with repeated measurements. Results are presented as means ± s.d. unless otherwise noted. Tests were performed with JMP 10 or SAS (SAS Institute, Cary, NC, USA).

Twenty-four weasels (four female, 20 male; 37–130 g) were tested for voluntary running; of these, five were also tested for V̇_O2,max. Several individuals did not use the voluntary wheel or ran in such brief bouts that the data were not usable. Among the weasels that spent substantial time running, most exercise bouts lasted less than 10 min and were followed by periods of inactivity (no wheel rotation and low and relatively stable V̇_O2). Although there was occasional activity within the cage (as indicated by peaks in V̇_O2 not associated with wheel movement), all weasels spent most of their time resting (e.g. Fig. 1).

Minimal RMR was strongly correlated with body mass (RMR_min in ml O₂ min^–1=0.105M^0.724, where M is mass in g; N=21, r²=0.744, P<0.0001; Fig. 2; mean mass=86.0±24.4 g, mean RMR_min=2.64±0.67 ml O₂ min^–1). Although sample size was small, V̇_O2,max in forced running was also correlated with body mass (V̇_O2,max=1.05M^0.701; N=5, r²=0.704, P=0.047; mean mass=89.1±29.5 g, mean V̇_O2,max=23.7±5.9 ml O₂ min^–1). Similarly, maximum voluntary V̇_O2 averaged over 1, 2 and 5 min intervals was correlated with body mass (0.189M^0.932, r²=0.50, P=0.003; 0.204M^0.905, r²=0.50, P=0.003; 0.171M^0.918, r²=0.48, P=0.006, respectively; N=14). The mass exponents for V̇_O2,max and RMR_min did not differ significantly (P>0.6). Mass exponents for maximum voluntary V̇_O2 were significantly higher than for RMR_min (P<0.014) but did not differ from that for V̇_O2,max (P>0.117), possibly because of low sample size for the latter.

We obtained acceptable voluntary running data for determining COT from 11 weasels (52.6–130 g, mean mass 98.1±22.7 g). Mean maximum speed for animals used for slope and intercept calculations was 2.8±1.1 km h^–1 (range 1.3–4.9 km h^–1). Measurements on these individuals lasted from 9.75 to 24 h. The mean distance run was 1.75±1.12 km and cumulative run time averaged 68.2±25.5 min, for a mean speed of 1.48±0.59 km h^–1. Nearly all wheel running activity occurred during daylight, but nine of the 11 measurements included less than one complete diurnal activity cycle (i.e. less than 12 h of daylight, which was approximately the ambient photoperiod for the majority of measurements). For these individuals, times and distances were scaled to 12 h of daylight by multiplying by 12 h and dividing by measurement hours, yielding a mean distance run per day of 1.94±1.15 km and a mean cumulative run time of 78.8±29.3 min. The maximum instantaneous speed (the fastest 1.5 s of running) averaged 5.1±1.1 km h^–1 (range 3.7–7.8 km h^–1). There was no relationship between body mass and any measure of running speed or distance (P>0.60).

Nine of the 11 speed versus V̇_O2 regressions were linear; two had significant quadratic terms (they tended to level out at high speeds). For these two individuals, addition of the quadratic term had little effect on predictive power (r² increased from 0.933 to 0.967 for male 119, and from 0.901 to 0.914 for male 130). Accordingly, for simplicity we used linear regressions for all individuals (e.g. Fig. 3); all were highly significant, with a mean r² of 0.71 (range 0.43–0.93).

This analysis included 118 running bouts by 18 weasels, including the 11 individuals used to calculate the relationship between V̇_O2 and speed. The mean bout duration was 3.99±2.26 min (range 0.725–10.8 min), the mean distance traveled per bout was 115±119 m (range 7–689 m) and the mean speed (=distance/duration) was 1.54±0.88 km h^–1 (range 0.25–4.01 km h^–1). Preliminary tests indicated that including individual ID as a random effect in a mixed model (to account for multiple measurements on individuals) did not improve model fit; accordingly, it was not included in subsequent analyses. A simple linear model including body mass (kg), mean speed (km h^–1) and distance (km) as predictors accounted for 90% of the variation in the amount of O₂ or energy consumed in a running bout (Table 1, Fig. 4). All predictors were highly significant (P<0.0001), as was the overall regression. The strongest predictor of running cost was distance traveled (Table 1). Regressions predicting the net cost of running (O₂ or energy consumed less RMR) were also highly significant (r²=0.761; Table 1). After accounting for the effects of size and speed, there was no difference in integrated running costs between the 11 animals used to calculate relationships between power and speed and the other seven weasels (ANCOVA; P=0.45).

As a comparison of the two models for calculating energy use during running, we regressed costs determined from distance, time and energy consumption (i.e. total kJ consumed, total km and mean km h^–1 per bout of running; Table 1) against costs predicted from speed, duration, and slopes and intercepts as described in Eqn 5. Body mass was included in both models. For all 118 bouts of running, the predicted and measured values were similar and highly correlated (r²=0.867, P<0.0001); a log₁₀ conversion slightly improved predictive power (r²=0.896). We also compared net costs (after subtracting RMR; Table 1, Eqn 6); again, results were highly correlated (r²=0.775, P<0.0001).

We obtained 832.4 h of tracking data from 35 weasels (mean body mass 99.2 g, range 61–133 g) in June through September in 1997–2006. Mean daily linear distance traveled by radiotracked animals was 1.32±0.83 km and mean daily activity time was 4.25±1.81 h. Their mean speed of movement, derived by dividing the linear distance traveled in the interval between successive position fixes by the duration of that interval, was 0.32±0.15 km h^–1. Ambient temperature (T_a) affects the activity and movement of weasels during summer (K.Z., M.K. and P.A.S., unpublished data). Therefore, we also calculated travel distances for the subset of tracking data when T_a was between 18 and 24°C, similar to conditions during laboratory COT measurements. At these temperatures, the mean daily distance traveled by 11 individuals was 1.45±0.59 km (N=24 observations), assuming linear travel between position fixes. Despite a lack of detailed knowledge of weasel locomotor behavior in the field, we can estimate energetic costs of transport. If wild weasels ran at the average speed observed for weasels in running wheels (1.54 km h^–1), a 96 g animal would have a total daily travel cost of 13.6 kJ (Table 1), and a net daily travel cost (excluding RMR; Table 1) of 9.0 kJ. Both of these estimates include postural costs. If only iCOT is considered (excluding both RMR and postural costs), the energy expended for travel would average 6.4 kJ day^–1.

Using radiotracking, Zub et al. (Zub et al., 2009) found an average duration of all types of activity of approximately 4 h day^–1, but there was considerable individual variation and some male weasels were active for as much as 10 h day^–1. Assuming that average running speed is constant and that the distance traveled is directly proportional to activity time, the most active males were traveling approximately 4.4 km day^–1, which would cost a 96 g animal 18.0 kJ day^–1 above RMR, or 12.8 kJ day^–1 (iCOT only).

Several studies of small mustelids (Scholander et al., 1950; Iversen, 1972; Moors, 1977; Casey and Casey, 1979) have reported unusually high basal or resting metabolic rates. Our findings (Fig. 2) are consistent with those results: minimal resting metabolism in Mustela nivalis – 2.86 ml O₂ min^–1 for an individual of the mean mass of 96 g – is considerably higher than the ca. 1.4–1.5 ml O₂ min^–1 predicted by either ‘classical’ least-squares (e.g. White and Seymour, 2003; White and Seymour, 2005) or phylogenetically adjusted (e.g. White et al., 2009) allometries for mammalian basal metabolic rate (BMR). We caution that the RMR we report are not directly comparable to BMR because our animals may not have been post-absorptive, and because T_a values in our study were below the estimated lower critical temperature of weasels [∼25°C (Casey and Casey, 1979)]. Nevertheless, our animals had access to (and used) insulative bedding and hence were probably in or close to thermoneutrality when resting.

There are few published data on maximal metabolic rate in mustelids. Weasels in our study had a forced-exercise V̇_O2,max approximately ninefold greater than RMR, and although our sample size for V̇_O2,max was small, the factorial aerobic scope (V̇_O2,max/RMR) is the same as the scope of 9 reported for exercised North American mink [Neovison (Mustela) vison (Williams, 1983)]. An aerobic scope of 9 is also consistent with results from other small mammals (e.g. Hinds et al., 1993; Weibel et al., 2004; Weibel and Hoppeler, 2005). The V̇_O2,max of weasels is ∼70% higher than predicted for mammals [fig. 1 in Weibel et al. (Weibel et al., 2004)], and the ‘normal’ aerobic scope stems from a proportionally high RMR in conjunction with the high V̇_O2,max. A possible confounding factor is the fact that our weasels were tested on a wheel and hence were not running on a flat surface (as is typical for exercise V̇_O2,max studies). However, a comparative analysis including >70 species revealed no difference between V̇_O2,max elicited on wheels versus that elicited on treadmills (E. L. Dlugosz, unpublished data).

A particularly interesting aspect of weasel biology is their extraordinary range of adult body mass [as much as fourfold (King, 1989; Zub et al., 2009)], which has obvious implications for energy requirements and ecology (Zub et al., 2011). A wide mass range is evident in our sample (Fig. 2) and permits estimation of intraspecific metabolic scaling. The scaling exponents for the upper and lower limits to aerobic metabolism (RMR and V̇_O2,max) in weasels are consistent with numerous studies of interspecific metabolic allometry in mammals (recent reviews in White and Seymour, 2004; White and Seymour, 2005; White et al., 2009). Both parameters show intraspecific scaling approximately to M^0.7–0.72 in weasels and do not differ from ‘typical’ scaling to M^0.75 or M^0.67. Although the scaling of V̇_O2,max in weasels (to M^0.701) is lower than the interspecific scaling to M^0.872 reported for 34 eutherian species (Weibel and Hoppeler, 2005), the difference is not significant. Curiously, the maximal V̇_O2 weasels attained in voluntary exercise scaled to a mass exponent (approximately M^0.91; Fig. 2) that was considerably (but not significantly) higher than the mass exponent for V̇_O2,max, and significantly higher than the mass exponent for RMR. We are unsure of the reason for this. One possibility is a size-related difference in position on the wheel during running (e.g. larger individuals might have a greater tendency than smaller animals to run ‘uphill’ and hence incur higher costs). We lack data to robustly test this idea, but observations of running weasels suggested that all individuals remained at or near the bottom of the wheels. Another possibility is size-related differences in gait or posture while running; again, we cannot formally test this hypothesis but our subjective impression is that there were no differences in gait or posture between small and large weasels.

Compared with a number of rodent species tested for voluntary locomotion in wheel respirometers, weasels were notable for their limited propensity to run. Total distances run per day were short, averaging less than 2 km, and bouts of running were brief and usually separated by long periods of inactivity (Fig. 1). In contrast, many rodents, including deer mice (Peromyscus maniculatus), California mice (P. californicus), laboratory mice (Mus domesticus), golden-mantled ground squirrels (Spermophilus lateralis), least chipmunks (Tamias minimus) and several other species of wild rodents, often run 5–12 km day^–1 in the same wheel systems (sometimes more) and running bouts may last for many minutes to hours (Chappell et al., 2004; Rezende et al., 2006; Chappell and Dlugosz, 2009; Dlugosz et al., 2012). The short running distances for weasels are somewhat surprising: carnivores generally have larger home ranges than non-carnivores (e.g. Kelt and Van Vuren, 2001) and hence might be expected to exhibit greater voluntary movement distances. Without additional data, it is unclear whether the difference is due to nonadaptive lineage divergence between rodents and carnivores, or results from differential selection on species with carnivorous versus herbivorous or omnivorous diets. In the latter context, we speculate that the short voluntary running distances we observed in the laboratory might reflect selection on weasels to minimize activity, both to conserve energy and to minimize exposure to predators (Korpimäki and Norrdahl, 1989; Zub et al., 2009). In that context, a potentially important factor is the high hunting efficiency of weasels in the Białowieza area: weasels in this area are often able to capture prey sufficient for their daily energy requirements in 1 to 2 h of active hunting (Zub et al., 2011). Field studies show that weasels preferentially use areas with high prey abundance, which increases their hunting efficiency and allows activity time to be minimized (Zub et al., 2008).

Radiotracking data from free-living weasels were consistent with the short voluntary movement distances in wheels. At ambient temperatures similar to those in the metabolic wheel tests, wild weasels moved an average of 1.45±0.83 km per day. That value is based on assumptions of linear movement between position fixes. Results from other species (Musiani et al., 1998; Rowcliffe at al., 2012), including another mustelid, the fisher [Martes pennanti (Powell, 1979)], indicate that radiotracking underestimates real movement distances by 30–90%. Assuming a correction factor of 50% (Powell, 1979), our free-living weasels traveled 2.2 km day^–1, quite similar to the 1.94 km day^–1 of wheel-running we observed in captive weasels.

Compared with allometric predictions of running costs derived from a broad range of terrestrial endotherms (Taylor et al., 1982), weasels in our wheel respirometers spent more energy than typical terrestrial runners when locomoting (Fig. 4). For example, when traveling at 4 km h^–1, a 96 g weasel has a metabolic rate of 14.6 ml O₂ min^–1 (Eqn 4, Fig. 5), while the metabolic rate predicted by the Taylor et al. (Taylor et al., 1982) allometry is 10.6 ml O₂ min^–1, a difference of 37%. The difference in energy cost is largely due to a higher intercept of the speed versus power regression: for a 96 g weasel, the slope (i.e. iCOT) is only 35% higher than predicted (144 versus 107 ml O₂ km^–1, respectively; Fig. 4), while the intercept is 80% higher than predicted [6.31 versus 3.51 ml O₂ min^–1, respectively; Eqn 4 (Taylor et al., 1982)]. Across all 11 animals for which we have slope and intercept values, intercepts differed significantly from predictions (P<0.001) but slopes did not (P=0.38). It is perhaps coincidental, but the magnitude of the difference between predicted and observed intercepts in weasels is close to the ca. 90% difference between their predicted and observed minimal metabolic rates. The ‘postural cost’ [intercept–RMR (Taylor et al., 1970; Taylor et al., 1982)] is also high in weasels: 3.45 ml O₂ min^–1 for a 96 g animal, compared with approximately 2.0 ml O₂ min^–1 predicted from an intercept of 3.51 ml O₂ min^–1 (Taylor et al., 1982) and a BMR of approximately 1.45 ml O₂ min^–1 derived from recent mammalian allometries (White and Seymour, 2003; White et al., 2009).

Other elongate mustelids also have high transport and postural costs during terrestrial locomotion. Like weasels, fishers and ferrets had roughly similar slopes but higher intercepts than expected from mass allometry (Taylor et al., 1982; Powell, 1979). Williams (Williams, 1983) found a higher than predicted energy cost of running in semi-aquatic American mink (800–1000 g), and again this was largely due to a high intercept (approximately twice the predicted value). Running costs in the even more aquatic North American river otter (11 kg) were also greater than predicted (Williams et al., 2002). Moreover, the phylogenetically distant but similarly semi-aquatic Australian water rat [Hydromys chrysogaster (Fish and Baudinette, 1999)] has a higher than expected cost of terrestrial locomotion, leading Williams et al. (Williams et al., 2002) to suggest that compromises inherent in species that must both run and swim lead to increased running costs.

In that context it is interesting that weasels, which have no morphological specializations or behavioral propensities for swimming, also have high running costs. This suggests that their short-legged elongate shape is responsible for the high COT. However, it is possible that the high costs we observed in weasels were an artifact of thermoregulatory expenditures. In small mammals running at temperatures below the thermal neutral zone, locomotor costs are often partially or fully additive to thermoregulatory expenditures, not substitutive, as is frequently the case in large mammals and birds (e.g. Wunder, 1970; Hart, 1971; Brooks and Fahey, 1984; Chappell et al., 2004; Webster and Weathers, 1990). As the weasels in our wheel respirometers were probably running at temperatures somewhat below their thermal neutral zone, the metabolic expenditures in excess of predicted values might be due to regulatory thermogenesis, not to transport costs per se. A counterargument is that some small mammals in the Taylor et al. (Taylor et al., 1982) data set may also have been running at sub-thermoneutral temperatures [22–27°C (Taylor et al., 1970)].

Like nearly all other species thus far tested during voluntary locomotion, weasels rarely ran at speeds that are predicted to require substantial anaerobic power production [some lactate accumulation often occurs at exercise intensities below V̇_O2,max (e.g. Brooks and Mercier, 1994)]. The estimated maximal aerobic speed [=(V̇_O2,max–intercept)/iCOT] of a 96 g weasel is 9.4 km h^–1. For the 11 animals used to generate COT data, the mean maximum speed averaged over 1 min was 3.3 km h^–1, and the maximum ‘instantaneous’ speed (the highest speed in a 1.5 s sample interval) averaged 5.3 km h^–1. The highest single instantaneous speed was 8.2 km h^–1 in a male weighing 104.7 g.

Gait changes as a function of speed (e.g. walking to running or bounding) have been reported for several small mammals, including elongate mustelids [mink (Williams, 1983); river otters, Lontra canadensis (Williams et al., 2002)] and a ground squirrel [Spermophilus saturatus (Kenagy and Hoyt, 1988)]. These transitions were associated with inflections in relationships between speed and metabolic rate. In much larger animals (horses), gait shifts may reduce costs of transport and peak musculoskeletal forces (e.g. Hoyt and Taylor, 1981; Wickler et al., 2003). In weasels, we observed walking (at low speed) and bounding (at high speed) both in the wild and in our wheel respirometers. However, COT data provided no clear evidence of changes in the speed versus power relationship at the speeds where gait transitions typically occurred (roughly 3–3.5 km h^–1). Gait-related shifts in power requirements were also lacking in two other mustelids tested in forced running on treadmills: a ferret [Mustela nigripes, 540 g (Taylor et al., 1982)] and two fishers [M. pennanti, 3–5 kg (Powell, 1979)]. Similarly, no inflections in speed versus power regressions have been reported in rodents tested during voluntary running [deer mice, California mice, laboratory mice, golden-mantled ground squirrels, least chipmunks and Mongolian gerbils (Chappell et al., 2004; Chappell et al., 2007; Rezende et al., 2006; Chappell and Dlugosz, 2009; Dlugosz et al., 2012)].

The importance of locomotor costs in animal energy budgets is of considerable interest to behavioral, community and conservation ecologists as well as to physiologists. Typically, it is assumed that energy acquisition is ultimately limiting and therefore the energy used for locomotion must be traded off against other life history components such as maintenance, growth and reproduction. Animals can adjust the energy expended on locomotion, but that plasticity is constrained by the need to move about the habitat to find food and perform other necessary behaviors. One approach for calculating the importance of locomotion expenditures is to use home range size to estimate daily movement distance (DMD) and measurements of COT to compute an ‘ecological cost of transport’ (ECOT) (Garland, 1983). If the ECOT is calculated as iCOT×DMD, the predicted costs for small mammals are very small [roughly 1% or less of DEE (Garland, 1983)]. However, laboratory and a few field studies of voluntary locomotion in small mammals often show considerably larger costs, ranging from 5% to more than 30% of DEE (Kenagy and Hoyt, 1989; Kenagy et al., 1989; Koteja et al., 1999; Chappell et al., 2004; Rezende et al., 2006; Chappell and Dlugosz, 2009). The difference stems in part from considerably greater DMD than predicted simply from home range dimensions, and because many studies include postural costs as well as iCOT in the total energy expended for movement.

Doubly labeled water measurements of free-living weasels in Białowieza indicate DEE of approximately 200 kJ day^–1 throughout the year, with an apparent trade-off between thermoregulatory and locomotor costs (Zub et al., 2009; Zub et al., 2011). Thus our estimates of average locomotor costs range from 3.2% of DEE (excluding postural costs and RMR) to 4.5% of DEE (including postural costs but excluding RMR). For the most active males, locomotor costs amounted to 6.4–9.0% of DEE. These transport costs are greater than the predicted ECOT of approximately 1% (Garland, 1983), but lower than values for wild and voluntarily running rodents (Kenagy and Hoyt, 1989; Kenagy et al., 1989; Koteja et al., 1999; Chappell et al., 2004; Rezende et al., 2006; Chappell and Dlugosz, 2009). Although their COT is higher than expected from body mass, weasels have considerably lower daily movement distances than have been reported for other small mammals. Accordingly, transport costs amount to a relatively minor fraction of weasel DEE. A potentially important caveat is that we do not know the distance weasels moved in burrows, or the energy costs of locomotion in burrows, which might be different from the cost of running in open areas.

The low daily expenditures by weasels for locomotion per se must be interpreted with caution when assessing the comprehensive energetic requirements of moving about the habitat. Our measurements of COT were taken in warm conditions, so costs of thermoregulation during movement were probably relatively minor. During winter in Białowieza, weasels outside of insulated nests experience environmental temperatures that require substantial regulatory thermogenesis (Casey and Casey, 1979; Jedrzejewski et al., 2000; Zub et al., 2009). Even in spring and autumn, temperatures in the early morning, when weasels begin activity, can be 5–10°C. We did not determine whether heat produced as a byproduct of locomotor exercise can be substituted for thermogenic heat requirements in weasels. However, in several small mammals, substitution is minimal or incomplete [e.g. thermogenic costs must be added to transport costs (Wunder, 1970; Hart, 1971; Wunder and Morrison, 1974; Chappell et al., 2004)], and it is reasonable to assume this is also the case for weasels. The high summed costs of activity and temperature regulation are probably important drivers for the quite low activity of weasels in winter, which is part of an apparent seasonal trade-off between activity and thermoregulation that results in surprisingly constant DEE throughout the year (Zub et al., 2009).

In conclusion, our study confirmed that the long-bodied and short-legged morphology of weasels is associated with high transport costs, as is the case in several larger elongate mustelids. The high transport costs are largely the result of high ‘postural costs’ and hence a high zero-speed intercept of the speed versus power relationship. The incremental cost of transport (the slope of the speed versus power relationship) is similar to predicted values. Weasels also have very high maximal rates of oxygen consumption, but because these are matched with unusually high RMR, the factorial aerobic scope of weasels falls within the range of values typical for mammals. Similarly, the mass scaling exponents of weasels’ lower and upper limits of aerobic metabolism are consistent with interspecific metabolic allometries of mammals. Although their energy costs during running are high, weasels have relatively short daily travel distances and times, presumably because of high hunting efficiency. As a result, metabolic costs of transport comprise a small fraction (∼5%) of DEE.

 
• BMR

  basal metabolic rate

 
• COT

  energy cost of transport

 
• DEE

  daily energy expenditure

 
• DMD

  daily movement distance

 
• E_c

  energy consumed

 
• ECOT

  ecological cost of transport

 
• E_net

  net energy consumption

 
• iCOT

  incremental cost of transport

 
• iV̇_O2

  ‘instantaneous’ oxygen consumption

 
• M

  body mass

 
• RMR

  resting metabolic rate

 
• v

  speed

 
• V̇_O2

  oxygen consumption

 
• V̇_O2,max

  maximal oxygen consumption

We are grateful for the assistance of the staff of the Polish Academy of Science Mammal Research Institute in Białowieza, and to the many visiting students who helped with trapping and radiotracking. The UC Riverside Biology Machine Shop constructed the running wheel respirometers.