ABSTRACT

The broad diversity in morphology and geographic distribution of the 35 free-ranging members of the family Canidae is only rivaled by that of the domesticated dog, Canis lupus familiaris. Considered to be among nature's most elite endurance athletes, both domestic and wild canids provide a unique opportunity to examine the variability in mammalian aerobic exercise performance and energy expenditure. To determine the potential effects of domestication and selective breeding on locomotor gait and economy in canids, we measured the kinematics and mass-specific metabolism of three large (>20 kg) dog breed groups (northern breeds, retrievers and hounds) of varying morphological and genomic relatedness to their shared progenitor, the gray wolf. By measuring all individuals moving in preferred steady-state gaits along a level transect and on a treadmill, we found distinct biomechanical, kinematic and energetic patterns for each breed group. While all groups exhibited reduced total cost of transport (COT) at faster speeds, the total COT and net COT during trotting and galloping were significantly lower for northern breed dogs (3.0 and 2.1 J kg−1 m−1, respectively) relative to hound (4.2 and 3.4 J kg−1 m−1, respectively) and retriever dogs (3.8 and 3.0 J kg−1 m−1, respectively) of comparable mass. Similarly, northern breeds expended less energy per stride (3.5 J kg−1 stride−1) than hounds or retrievers (5.0 and 4.0 J kg−1 stride−1, respectively). These results suggest that, in addition to their close genetic and morphological ties to gray wolves, northern breed dogs have retained highly cursorial kinematic and physiological traits that promote economical movement across the landscape.

INTRODUCTION

All domestic dogs (Canis lupus familiaris) are recent and exclusive decedents of gray wolves, Canis lupus Linnaeus 1758, having been domesticated in the last 15,000–30,000 years (Freedman et al., 2014; Skoglund et al., 2015; Wang et al., 2016). However, among the nearly 400 breeds representing modern dogs (Kleiman et al., 2003), unique artificial selection trajectories (Galibert et al., 2011; Jimenez, 2016) have resulted in extreme morphological diversity that exceeds that for the remainder of the family Canidae (Clutton-Brock, 1999; Lindblad-Toh et al., 2005; Vaysse et al., 2011; Wayne, 1986, 2001; Wilcox and Walkowicz, 1995). In recent years, much emphasis has been placed on elucidating the origins of dog domestication from genomic (e.g. Freedman et al., 2014; Parker, 2012; Skoglund et al., 2015; Vonholdt et al., 2010) to zooarcheological (Perri, 2016; Pionnier-Capitan et al., 2011), morphometric (Drake et al., 2015) and biogeographical evidence (Larson et al., 2012). By comparison, little is known about the effects of extensive artificial selection on physiological performance and metabolic demands of the different breeds of dog (but see Bermingham et al., 2014; Careau et al., 2010; Speakman et al., 2003).

With the highest sustained metabolic rates on record (approximately 4400 J kg−1 day−1 while racing 490 km in 3 days at approximately −20°C; Hinchcliff et al., 1997), canids are considered among the most elite endurance athletes in the natural world (Miller et al., 2015; Poole and Erickson, 2011; Snow, 1985). This compares with approximately 3900 J kg−1 day−1 for lactating mice raising artificially large litters (14 pups) in a cold environment (5°C; Hammond et al., 1994), 2000 J kg−1 day−1 for thoroughbred horses during heavy training (Lewis, 1995; Pagan and Hintz, 1986) and 1400 J kg−1 day−1 for Tour de France cyclists (Westerterp et al., 1986). Dogs, coyotes, wolves and foxes exhibit aerobic performance capacities roughly three times greater than those of equivalently sized terrestrial mammals (Seeherman et al., 1981; Taylor et al., 1987a; Weibel and Hoppeler, 2005; Weibel et al., 1983, 2004). Dogs, for example, have aerobic scopes [the ratio of maximum oxygen uptake (O2,max) to basal metabolic rate] of 20–30, compared with aerobic scopes of about 10 for goats of equal body mass (Weibel et al., 1987). To facilitate this greater oxygen capacity, dogs possess structural and functional adaptations at each step in the pathway for oxygen, including in the muscle mitochondria, muscle microvasculature, heart and lungs (reviewed in Taylor et al., 1987b). Together, the wide aerobic scopes exhibited by canids are consistent with an ability to run for extended periods at sustained speeds without becoming anaerobic (Koteja, 1987; Okarma and Koteja, 1987).

Given these physiological and morphological characteristics, both domestic and wild canids provide a unique opportunity to investigate mammalian exercise performance and energy expenditure. The expectation is that aerobic capacity provides a selective advantage for wild canids (Okarma and Koteja, 1987). In the wild, the rates at which individuals acquire, transform and expend energy (i.e. their metabolic rates) are integrative measures of organism function that have fundamental consequences for survival and reproductive success (Brown et al., 2004; Halsey, 2011). For many highly mobile species such as canids, the energetic costs associated with activity and movement form a substantial portion of daily energy expenditure (Boisclair and Leggett, 1989; Garland, 1983; Girard, 2001; Gorman et al., 1998; Karasov, 1992; Rezende et al., 2009; Scantlebury et al., 2014; Tatner and Bryant, 1986; Weibel et al., 2004). In wolves and dogs, movement costs are superimposed on elevated energy demands associated with large body size (Peters, 1983), endothermy (Bennett and Ruben, 1979) and carnivory (Carbone et al., 2007, 2011), suggesting a key selective advantage for minimizing locomotor costs.

List of symbols and abbreviations
     
  • CoM

    center of mass

  •  
  • COT

    cost of transport (J kg−1 m−1)

  •  
  • COTnet

    net cost of transport (J kg−1 m−1)

  •  
  • COTtot

    total cost of transport (J kg−1 m−1)

  •  
  • RMR

    resting metabolic rate (ml O2 kg−1 min−1)

  •  
  • tc

    foot contact time (s)

  •  
  • O2

    rate of oxygen consumption (ml O2 kg−1 min−1)

Here, we examined how selective breeding and domestication may have disrupted the optimization of these locomotor costs and altered the economy of movement in domestic dogs. This was accomplished by comparing the locomotor kinematics and energetics of three large (>20 kg) breed groups along a continuum of relative genetic and morphological proximity to gray wolves. Northern breed individuals included Siberian huskies, Alaskan malamutes and Samoyeds. These ‘sled dogs’ are among the oldest domestic dog breeds (Huson et al., 2010; Parker, 2012; Wang et al., 2013) and possess the most lupine traits (i.e. bear the greatest morphological and genomic resemblance to their wild progenitor, the gray wolf; Mech, 1970; Parker et al., 2004; Skoglund et al., 2015; Udell et al., 2010; Vonholdt et al., 2010). Northern breeds have been traditionally used to assist humans with long-distance activities including arctic hunting expeditions and sledge pulling (Rennick, 1987). Scent hounds, such as the Plott hounds measured in the present study, were primarily bred to aid hunters by tracking the scent of wild game (American Kennel Club, 2006), an activity that requires speed but only intermediate levels of aerobic endurance relative to northern breeds. Retrievers (e.g. golden, labrador, flat-coated) were also bred to assist in hunting, but typically require shorter, largely anaerobic bouts of activity to retrieve killed or injured game (American Kennel Club, 2006). Because the genomic and morphological effects of dog domestication have been described (e.g. Drake et al., 2015; Freedman et al., 2014; Parker, 2012; Skoglund et al., 2015), our goal was to assess the coincident energetic consequences of human-induced selective pressures for various physical traits (e.g. limb length, body mass) and desired tasks (e.g. guarding, hunting, pulling loads). We found that working breeds of dogs most similar to wolves (i.e. northern breeds) have lower metabolic transport costs than hounds and retrievers, which have undergone divergent artificial selection trajectories from this wild canid progenitor.

MATERIALS AND METHODS

Study design

We quantified the overground stride mechanics, kinematics and preferred speeds of steady-state walking, trotting and galloping in three breed groups of domestic dogs differing in genomic relatedness to the gray wolf. These data were then paired to the gait-specific metabolic demands of level exercise for these animals measured by open-flow respirometry. Metabolic rates across each gait, total and net cost of transport, as well as the cost per stride were used to compare overall locomotor energy economy across the dog breeds. Assuming that the genetic distance from wolves approximates the relative extent of domestication (Parker, 2012), we then used the breed-specific data to assess the potential effect of increased domestication on the economy of movement in dogs.

Animals

The study consisted of 23 healthy, adult dogs (2–11 years old) in three breed categories: northern breeds (N=9), hounds (N=7) and retrievers (N=7; Table 1).

Table 1.

Summary of morphological characteristics for the dogs examined in this study

Summary of morphological characteristics for the dogs examined in this study
Summary of morphological characteristics for the dogs examined in this study

All dogs were deemed healthy, active and without any known impairments that might influence locomotion. To ensure adequate conditioning and mitigate training effects associated with the study protocol, all subjects participated in routine outdoor exercise and were physically trained for at least 1 month prior to and throughout data collection. Informed written consent, animal age and health history were obtained from all dog owners, and the study protocol was approved by the UC Santa Cruz Institutional Animal Care and Use Committee.

Gait mechanics and kinematic data

To determine the physiological basis of gait selection and preferred performance parameters (Kar et al., 2003; Nanua and Waldron, 1995; Perry et al., 1988), we analyzed the natural, unrestrained locomotor gaits of each dog with repeated outdoor kinematic trials. During each trial, dogs walked, trotted and galloped at steady-state speed along a 10 m transect of level ground while being filmed by high-speed (Casio EX-F1, 300 frames s−1) and high-definition (Sony HDR-CX290/B, 1080 HD, 60p) video cameras mounted perpendicular to the test course and in the dog's cranial–caudal sagittal plane.

Videos were analyzed (Corel VideoStudio ProX5, Ottawa, ON, Canada) for animal speed and basic stride mechanics (stride length, stride frequency). Given the dynamic and geometric similarity of the subjects (Alexander, 1984, 2005; Alexander and Jayes, 1983), dimensionless Froude numbers (speed2/limb length×gravitational acceleration) were computed for gait transitions to compare breeds after accounting for limb length. We excluded from analysis all passes in which the dog visibly changed gait or speed mid-transect, turned its head, or otherwise deviated from a straight-line path. The preferred range of speeds for each gait was then calculated for each animal and used to ensure that subsequent metabolic treadmill trials approximated the preferred walking, trotting and galloping speeds of the individual dog.

Previous studies report that, overall, dog sagittal-plane gait patterns on a level treadmill do not differ from those of overground locomotion (Torres et al., 2013), although the stance phase is slightly longer (Fischer and Lilje, 2011). We tested these findings, and closely examined gait kinematic differences across breeds, using a random subset of at least four dogs within each breed group. Anatomical landmarks on the limb joints were determined via manual palpation while flexing and extending each joint, then digitized and tracked at 300 Hz from high-speed videos (Tracker Video Analysis and Modeling Tool, http://physlets.org/tracker/) to measure 24 biomechanical and kinematic parameters (Table 2; Table S1) from the subjects moving overground and on the treadmill at the same gait and speed (±10%).

Table 2.

Kinematic parameters of each gait for northern breed, hound and retriever groups (N=4 for each group)

Kinematic parameters of each gait for northern breed, hound and retriever groups (N=4 for each group)
Kinematic parameters of each gait for northern breed, hound and retriever groups (N=4 for each group)

Metabolic measurements and energetic costs

Because animals change gaits to achieve stability and minimize energetic costs of movement (Biewener, 1990; Cavagna and Kaneko, 1977; Hoyt and Taylor, 1981; Hoyt et al., 2006), we compared gait-specific metabolic demands across breed groups. We took simultaneous kinematic and metabolic measurements during level treadmill running for a subset of dogs according to Williams et al. (2002). For each dog, the rate of oxygen consumption (O2, ml O2 kg−1 min−1) during rest and each gait was measured by an integrated open-flow respirometry system (TurboFOX-RM, Sable Systems International, Las Vegas, NV, USA). Following an overnight fast to ensure post-absorptive state, each animal was conditioned to rest (standing stationary or lying still in sternal recumbency), walk, trot and gallop inside a reinforced Plexiglas metabolic chamber (1.6 m×0.5 m×1 m) mounted on the surface of a variable-speed treadmill (Q65, Quinton Instrument Co., Bothell, WA, USA). The chamber was equipped with a fan to facilitate rapid mixing of expired gas and prevent overheating of exercising dogs. Each dog was weighed (Aryln 320D, East Rockaway, NY, USA) prior to every exercise trial, and air temperatures averaged 23.4°C (range 22–25°C) within the chamber during measurements. These temperatures fell within the thermoneutral zones of these breeds (National Research Council, 2006; Speakman et al., 2003). To ensure that the animals reached a physiologically stable state, each randomized exercise trial lasted a minimum of 12 min; sessions that included a pre-exercise resting metabolic rate (RMR) measurement lasted approximately 25 min.

Chamber air was drawn through the system with an integrated vacuum pump at a flow rate of 230 l min−1. At this flow rate, the fractional concentration of oxygen in the chamber remained above 0.2040 to avoid hypoxic conditions. Sub-samples of air from the exhaust port of the chamber were drawn through a series of six columns, alternatingly filled with desiccant (Drierite, W. A. Hammond Drierite, Xenia, OH, USA) and CO2 scrubber (Sodasorb, W.R. Grace & Co, Chicago, IL, USA) before entering an oxygen analyzer. The main flow rate through the chamber, percentage of oxygen in the expired air, humidity of the gas sample and barometric pressure were monitored continuously and recorded once per second on a computer using Expedata software (Sable Systems International). All values were corrected to standard temperature and pressure, dry (STPD), and the entire system was calibrated daily with ambient air (20.95% O2 at sea level where trials occurred) and with dry N2 gas to test for chamber mixing and leaks according to Fedak et al. (1981).

For each trial, average O2 was calculated using eqn 4b from Withers (1977) and an assumed respiratory quotient of 0.82 for dogs consuming a conventional, mixed diet (Raab et al., 1976; Speakman et al., 2003). Physiological measurements, including energetic cost per kilogram per unit distance (cost of transport, COT; J kg−1 m−1) and cost per stride (J kg−1 stride−1), were derived from speed and stride frequency, respectively, using an energy conversion of 20.1 J ml−1 O2, assuming a negligible contribution from anaerobic glycolysis (Schmidt-Nielsen, 1997; Taylor et al., 1982). Total cost of transport (COTtot) was derived from the slope of the energy expenditure–speed relationship for each breed, i.e. COTtot was calculated for each trial measurement by dividing mass-specific metabolic cost by the trial speed. Net cost of transport (COTnet) was calculated by subtracting the mean RMR of each individual from the energetic cost of the trial, then dividing by trial speed. Both COTtot and COTnet include any postural costs during locomotion (the difference between mean RMR and the y-intercept in the energy expenditure–speed relationship; Halsey, 2013, 2016).

During the metabolic measurements on the treadmill, we recorded stride length and stride frequency using high-speed and high-definition cameras (described above) mounted in the sagittal plane on the right side of each dog at a distance of 1.65 m. The timing intervals for sequential cycles of the right forelimb were averaged from the video sequences, and the number of strides taken per second was calculated for each gait (Williams et al., 2002).

Statistical analysis

Statistical analyses and figures were produced using JMP Pro12 (SAS Institute Inc., Cary, NC, USA) and R (v. 3.1.1, https://www.r-project.org/). We used principle components analysis (PCA) and linear discriminant analysis (LDA) in tandem to compare kinematic parameters across breed groups while controlling for locomotor gait. To determine the potential effect of the treadmill on kinematics, we performed paired Student's t-tests (two-tailed) comparing the stride frequency and stride length for treadmill and overground locomotion within the same individual and breed group. Differences in age (years), body mass (kg) and limb length (m) between groups were determined by one-way analysis of variance (ANOVA) followed by Tukey–Kramer honest significant difference (HSD) tests. We also used ANOVA with HDS to compare mass-specific O2 and stride mechanics by gait across groups. Predicted (Heglund and Taylor, 1988) and measured preferred speeds for each gait, and transitions between gaits, were compared using paired Student's t-tests. We used analysis of covariance (ANCOVA) and least square linear regressions to determine the relationships between running speed and mass-specific metabolic rate, stride frequency and stride length for each individual and breed group. For all linear models, we checked the assumptions of linearity, normality and homoscedasticity by visual inspection of plotted residuals. To examine differences in metabolic COT across breeds, we fitted a three-parameter exponential decay model and determined whether 95% confidence intervals for each breed group overlapped with the estimates of the other two groups. All model combinations were fitted with best model fits based on the lowest Akaike information criteria corrected for small sample size (AICc), and study results are expressed as the mean±s.e.m. (α=0.05, a priori).

RESULTS

Gait mechanics

Dog breed groups did not differ significantly from one another in age (F2,20=0.07, P=0.93), body mass (F2,20=3.0, P=0.07), forelimb length (i.e. withers or shoulder height above ground; F2,17=3.18, P=0.07) or hindlimb length (hip height above ground; F2,17=2.81, P=0.09; Table 1). However, dog breed groups differed significantly in several of the basic overground stride mechanics measured (Table S2). For example, there was wide variation in the range of speeds selected for each gait (walk, trot and gallop) across breed groups (Fig. 1; Table S2). Relative to hounds, northern breeds walked, trotted and galloped over a broader range of speeds. Retrievers showed a contracted speed range for trotting but the largest breadth of galloping speeds. According to the average travel speed for each gait, the three breed groups did not differ from one another while walking (F2,134=0.28, P=0.76), but did for faster gaits (Table S2). Retrievers trotted at significantly faster speeds than hounds (t119=1.97, P=0.01) but not northern breeds (t168=1.97, P=0.13). Furthermore, mean galloping speed was faster for retrievers than for both hounds and northern breeds (F2,211=17.83, P<0.001; Table S2). Across groups, walk–trot transition speeds (F2,20=0.22, P=0.81) and Froude numbers (F2,18=1.1, P=0.36) did not differ across groups, indicating locomotor similarity at slow speeds. However, at the physiologically equivalent transition from trotting to galloping (Taylor et al., 1982), retrievers ran at faster speeds (F2,20=4.19, P=0.03) and with higher Froude numbers (F2,17=5.27, P=0.02) than did northern breeds or hounds.

Fig. 1.

Variation in the range of speeds selected for walking, trotting and galloping by northern breed, hound and retriever dogs. Box-and-whisker plots depict group-wide speed ranges (walking, white; trotting, gray; galloping, black), with the median denoted as the vertical line within each gait range quartile box. Outliers are depicted as individual points beyond the associated quartiles.

Fig. 1.

Variation in the range of speeds selected for walking, trotting and galloping by northern breed, hound and retriever dogs. Box-and-whisker plots depict group-wide speed ranges (walking, white; trotting, gray; galloping, black), with the median denoted as the vertical line within each gait range quartile box. Outliers are depicted as individual points beyond the associated quartiles.

Hounds (t6=5.02, P<0.01) and retrievers (t6=2.56, P=0.04), but not northern breeds (t8=1.4, P=0.2), trotted at speeds significantly faster than predicted for quadrupeds of similar body mass (Heglund and Taylor, 1988). Hounds and retrievers also transitioned from trot to gallop at speeds that were faster than predicted by body mass (18–26% faster, P<0.01; Fig. 2). Only retrievers exhibited preferred galloping speeds faster than those predicted by Heglund and Taylor (1988) (t6=2.83, P=0.03).

Fig. 2.

Comparison of predicted and measured physiologically equivalent trot–gallop transition speeds. (A) Northern breed, (B) hound and (C) retriever dogs. The figure shows stride frequency in relation to locomotor speed while moving on a level outdoor transect. Each data point is a single measurement for a test run by an individual dog. Dash–dot lines represent the minimum and maximum range of the data across speeds. The gray box denotes the difference between measured (dashed vertical line) and predicted (dotted vertical line) (Heglund and Taylor, 1988) trot–gallop transition speeds for each breed. Pseudo-linearity of data within each group is caused by limited variation of speed–stride frequency measurements resulting from the 10 m outdoor transect length used during data collection.

Fig. 2.

Comparison of predicted and measured physiologically equivalent trot–gallop transition speeds. (A) Northern breed, (B) hound and (C) retriever dogs. The figure shows stride frequency in relation to locomotor speed while moving on a level outdoor transect. Each data point is a single measurement for a test run by an individual dog. Dash–dot lines represent the minimum and maximum range of the data across speeds. The gray box denotes the difference between measured (dashed vertical line) and predicted (dotted vertical line) (Heglund and Taylor, 1988) trot–gallop transition speeds for each breed. Pseudo-linearity of data within each group is caused by limited variation of speed–stride frequency measurements resulting from the 10 m outdoor transect length used during data collection.

Kinematics

After controlling for individual, gait and speed, we found no consistent effect of the treadmill relative to overground locomotion on sagittal plane joint flexion and extension (Torres et al., 2013) and therefore assumed treadmill trials were representative of free-ranging dog locomotion. While not significantly different (P=0.07–0.09 range), limb lengths were generally shorter in hounds than in other breeds (Table 1). To account for this, we used relative limb protraction and retraction length values (dividing by limb length of each dog) in subsequent analyses (Table 2). After using PCA and LDA to condense the initial set of 24 measured kinematic parameters down to 18 variables loaded onto 5 factors as determined by eigenvalues >1, we detected group-wide differences in trotting (Wilk's λ=0.002, P=0.038), but not walking (Wilk's λ=0.042, P=0.88) or galloping (Wilk's λ=0.002, P=0.35). Upon closer analysis of each gait with ANOVA, we found that, relative to hounds and retrievers, northern breeds had the greatest vertical displacement while walking (5.2±1.4 cm, F2,17=5.0, P=0.02), and that this displacement exceeded that of their trot (4.5±0.9 cm; Table 2). While trotting, forelimb retraction length was greater in hounds than in retrievers (t13=2.1, P<0.01), and forelimb retraction angle was greatest in hounds relative to both other groups (F2,18=10.54, P<0.01; Table 2). During gallop, northern breeds showed longer forelimb stance durations (F2,10=17.27, P<0.001) and protraction lengths (F2,10=5.94, P=0.02) than hounds and retrievers (Table 2). In contrast, the duration of the forelimb galloping swing phase was significantly longer for retrievers than for northern breeds (t10=2.23, P<0.01; Table 2).

Energetics

Because body mass differences between groups can bias mass-specific comparisons of oxygen consumption (Packard and Boardman, 1999), we first tested for a possible effect of mass. We used ANCOVA with resting oxygen consumption as the dependent variable, breed group as the main factor and body mass as a covariate. The general linear model was highly significant (GLM: F5,183=8.2, P<0.01), but body mass was not a significant covariate (mass: d.f.=1, F=2.5, P=0.12), nor was its interaction with breed group significant (breed×mass interaction: d.f.=2, F=2.9, P=0.08). We therefore assumed that mass-specific oxygen consumption rates appropriately account for the effect of body mass within the comparatively small mass range of the dogs in our study. We used these rates for all subsequent analyses to compare energy demand of the dogs with data from other studies typically reporting O2 on a mass-specific level.

For all dogs, mass-specific metabolic rate increased linearly as a function of locomotor speed (Fig. 3), as described previously for wild and domesticated canids (e.g. Taylor et al., 1982; Weibel et al., 1983) and the majority of other terrestrial quadruped species (Taylor et al., 1982), according to:
formula
(1)
formula
(2)
formula
(3)
Fig. 3.

Mass-specific oxygen consumption plotted as a function of locomotor speed for northern breed, hound and retriever dogs. Each data point is a single O2 trial measurement from a dog moving on the level treadmill at a given speed. Trials were repeated across the full range of speeds for each individual, as determined by prior outdoor running tests. The slopes of the regression lines are net cost of transport (COTnet) for each breed and are presented in Eqns 1–3.

Fig. 3.

Mass-specific oxygen consumption plotted as a function of locomotor speed for northern breed, hound and retriever dogs. Each data point is a single O2 trial measurement from a dog moving on the level treadmill at a given speed. Trials were repeated across the full range of speeds for each individual, as determined by prior outdoor running tests. The slopes of the regression lines are net cost of transport (COTnet) for each breed and are presented in Eqns 1–3.

where O2 is in ml O2 kg−1 min−1 and speed is in m s−1. Hounds had elevated mass-specific O2 across the range of measured trial speeds relative to both northern breeds and retrievers (Fig. 3). Consequently, gait-specific metabolic demands were higher for hounds while walking and trotting (F2,50=4.7, P<0.01 and F2,83=16.0, P<0.01, respectively), although galloping energetics did not differ across breeds (F2,5=1.1, P=0.41). Hounds also exhibited higher and longer mass-specific stride frequencies and lengths, respectively, than retrievers and northern breed dogs during treadmill locomotion.

COTtot (J kg−1 m−1), which includes locomotor, postural and maintenance costs associated with each animal's RMR (Schmidt-Nielsen, 1972; Williams, 1999), decreased with speed for all individuals within and among dog breed groups (Fig. 4A). Those breeds moving at faster running speeds maximized transport economy. At comparable speeds, northern breeds exhibited lower COTtot than both hounds and retrievers, as indicated by the significantly lower asymptote in our 3-parameter exponential decay model (Table S3). Compared with COTtot of all running mammals (including other canids) presented in Taylor et al. (1982), transport costs for northern breeds were considerably lower than predicted by body mass (Fig. 5). COTnet, which includes locomotor demands (including those associated with the posture evoked during locomotion; Halsey, 2016), but not RMR, was also lowest for northern breeds (Fig. 4B; Fig. S1, Table S3). Overall, relative metabolic costs associated with both maintenance and locomotion were lowest for northern breeds as mass-specific resting costs were similar (approximately 6–8 ml O2 kg−1 min−1) across breed groups; Fig. S1).

Fig. 4.

Mass-specific energetic costs associated with the cost of transport and cost per stride. (A) Total cost of transport (COTtot), (B) COTnet and (C) cost per stride for running dogs. Three locomotor gaits for northern breeds, hounds and retrievers were compared. Boxes not connected by a dashed line differ significantly (P<0.05). Total COT was lowest while galloping for all groups, and northern breeds had significantly lower COTnet and step costs than hounds and retrievers, particularly while trotting.

Fig. 4.

Mass-specific energetic costs associated with the cost of transport and cost per stride. (A) Total cost of transport (COTtot), (B) COTnet and (C) cost per stride for running dogs. Three locomotor gaits for northern breeds, hounds and retrievers were compared. Boxes not connected by a dashed line differ significantly (P<0.05). Total COT was lowest while galloping for all groups, and northern breeds had significantly lower COTnet and step costs than hounds and retrievers, particularly while trotting.

Fig. 5.

COTtot for various canids in relation to the allometric regression ofTaylor et al. (1982)for running mammals: COTtot=10.7×mass−0.32 (dashed line). Filled triangles are data from the present study; open symbols represent data from dogs (breeds not specified) and African wild dogs running on a level treadmill as presented in Taylor et al. (1982). All dogs measured in the present study had lower transport costs than predicted by body mass, and this was particularly true for the northern breed dogs.

Fig. 5.

COTtot for various canids in relation to the allometric regression ofTaylor et al. (1982)for running mammals: COTtot=10.7×mass−0.32 (dashed line). Filled triangles are data from the present study; open symbols represent data from dogs (breeds not specified) and African wild dogs running on a level treadmill as presented in Taylor et al. (1982). All dogs measured in the present study had lower transport costs than predicted by body mass, and this was particularly true for the northern breed dogs.

Faster speeds significantly reduced the mass-specific energy cost per stride (J kg−1 stride−1) for hounds (cost per stride=−0.299×speed+5.49, r2=0.14, N=29, P=0.05) but not retrievers (P=0.11) or northern breed dogs (P=0.7). Across all speeds, the mean metabolic cost per stride was significantly lower for northern breeds (3.47±0.09 J kg−1 stride1) than retrievers (3.84±0.12 J kg−1 stride−1) and hounds (5.00±0.15 J kg−1 stride−1; P=0.05 and P<0.01, respectively; Fig. 4C). Indeed, energetic demands associated with trotting in northern breeds were significantly lower than those of walking and galloping (F2,67=6.7, P<0.01; Fig. 4), indicating the metabolic economy of trotting relative to both slower and faster gaits in this group. Forelimb and hindlimb foot contact times (tc) were positively related to these costs per stride in hounds (cost per stride=3.13+4.64tc, r2=0.84, P<0.01; cost per stride=3.17+4.5tc, r2=0.89, P<0.01, respectively), but had no effect on retriever and northern breed dogs (P=0.67–0.82 range).

DISCUSSION

Although dogs in general possess a suite of adaptations for aerobic locomotion (reviewed in Taylor et al., 1987b), the between-group differences we observed in the present study reflect a physiological signature of artificial selection in the economy of running by different dog breeds. We found that that this was manifested as breed-specific differences in both overground stride mechanics and treadmill-derived movement energetics among northern breed, hound and retriever groups. Thus, faster speeds promoted maximum economy for all dogs, but northern breeds had the lowest COTtot, COTnet and cost per stride levels relative to hounds and retrievers when trotting and galloping (Fig. 4).

Our hypothesis, that dog breeds more closely related to their gray wolf progenitor have relatively lower COT, was empirically supported (Fig. 4; Fig. S1, Table S3). Hounds and retrievers are both relatively modern breeds compared with the ancient lineage that includes northern breed dogs (Huson et al., 2010; Parker et al., 2004; Vonholdt et al., 2010; Wang et al., 2013). Genetically, the ancient breeds cluster together closest to gray wolves, but the group is surprisingly diverse in morphology and origin. This group includes the akita and chow chow of Asian origin, the saluki and Afghan hounds from the Middle East, the African basenji, and the northern breeds we assessed (Parker, 2012). Our study suggests that over the last ≥15,000 years of domestication, selective breeding has altered the aerobic locomotor economy of dogs, with the northern breeds retaining an economical physiological foundation that originated with gray wolves. To date, the limited existing data on the metabolic cost of running in wolves (Taylor et al., 1982; Weibel et al., 1983) does not indicate superior locomotor energy economy in wolves. However, comparisons with the current study may be misleading as a result of the adult ages of our dogs and the immature age of the wolves in the previous studies. Consequently, additional studies that measure ecologically relevant metabolic rates of adult wolves at endurance speeds are needed to determine the similarities or differences in locomotor energetics of wolves and domesticated dogs of comparable morphology and age.

To determine whether interbreed differences in energetic costs per stride were related to variation in gait patterns, we compared the Froude numbers for each breed at the walk–trot and trot–gallop transition speeds. Previous work has shown that animals of different masses but moving at the same Froude number are dynamically similar, and hence use the same gait, have comparable foot phase relationships, relative stride lengths and duty factors, and exert similar ground reaction forces (Alexander, 1984, 2005; Alexander and Jayes, 1983). At the walk–trot gait transition, our results reflected those of prior studies (e.g. Jayes and Alexander, 1978; Maes et al., 2008) where dogs began trotting at Froude numbers ≤0.5. However, dogs in our study began galloping at Froude numbers around 1 (mean=0.93±0.07), much lower than the predicted Froude numbers (≥3) reported in the previous studies. Both lower sample sizes and space constraints of the previous studies (Jayes and Alexander, 1978; Maes et al., 2008) may have contributed to these differences in Froude numbers when comparing our trials of 23 individual dogs running off-leash along an outdoor course.

When compared with the gait mechanics predictions of Heglund and Taylor (1988), we found that hounds and retrievers, but not northern breeds, trotted and transitioned from trot to gallop at speeds significantly faster than expected based on body mass (Fig. 2). The original study by Heglund and Taylor (1988) developed allometric equations concerning the effects of body size on stride mechanics from 16 species of wild and domestic quadrupeds ranging in mass from 30 g mice to 680 kg horses. Domestic dogs represented the only carnivore species in their analysis. It is noteworthy that in the present study, the two breed groups that differed significantly from the predicted mechanics, the hounds and retrievers, also showed significantly higher mass-specific COT and stride costs for these gaits than northern breed dogs (Fig. 4). In contrast, the stride mechanics of the northern breeds were as predicted. Overall, centuries of selective breeding for hunting performance in hounds and retrievers may have increased the preferred speed range for these breeds (Fig. 1; Table S2), with ensuing reduced locomotor economy (Fig. 4; Table S3).

Despite differences in basic stride mechanics across breeds, detailed kinematic analyses revealed limited distinctions between groups. Based on 24 kinematic parameters, we found larger forelimb retraction lengths and angles while trotting for hounds compared with northern breeds and retrievers (Table 2). This wider forelimb swing resulted in longer stride lengths and faster stride frequencies for hounds, which may have contributed to their higher COT and stride costs while trotting (Fig. 4). In contrast, northern breeds were the only group in which the mass-specific stride costs associated with trotting were significantly lower than those of both walking and galloping (Fig. 4C), resulting in relative energy economy for this intermediate-speed gait. This group also exhibited reduced vertical displacement while trotting compared with walking (Table 2). Such ‘spring dampening’ while loading the Achilles tendon at speed reduces damaging vibrations and enhances forward propulsion with subsequent energy savings (Alexander, 2001; Hermanson, 1997; Reilly et al., 2007; Wilson et al., 2000, 2001), which is consistent with our metabolic measurements (Fig. 3).

More generally, most terrestrial quadrupeds exhibit two unique mechanisms for reducing muscular work, and hence energy expenditure, during locomotion: pendular and mass-spring dynamics (Biewener, 2006; Cavagna and Kaneko, 1977; Cavagna et al., 1977; Hoyt et al., 2006). At walking speeds, animals exchange kinetic energy with potential energy of their center of mass (CoM) through an inverted pendulum mechanism (Cavagna et al., 1977; Griffin et al., 2004). Pendular energy savings persist even for loaded and incline locomotion (Gomeñuka et al., 2014; Pontzer, 2016), although the benefits of this mechanism diminish at faster speeds (Gomeñuka et al., 2016). For running gaits, a spring–mass mechanism predominates, where stretched elastic structures (ligaments and tendons) store and recover mechanical energy (Alexander, 1988; Blickhan, 1989; Cavagna et al., 1977, 1988). In the present study, the economical trotting gait of northern breed dogs likely suggests optimized spring–mass energy savings compared with other breeds. This is consistent with observations of these animals during endurance activities and races. For example, Greenland sled dogs are capable of trotting at 2.5 m s−1 for 8–10 h each day for 2–3 days, covering 60–80 km daily (Gerth et al., 2010). Similarly, wolves routinely travel in the trotting gait at the same speed (2.4 m s−1; Mech, 1994) and can cover 76 km in 12 h (Mech and Cluff, 2011).

Foot tc, described as the stride's stance phase duration, decreases as a power function of speed (Hoyt et al., 2000) and has been shown to be inversely related to the energy expended per stride (Alexander and Ker, 1990; Kram and Taylor, 1990). Regardless of differences in the COT, we found no significant difference in hindlimb kinematics, including tc, across gaits for the three dog breed groups (Table 2). Rather than limb kinematics per se, body posture and its relationship to kinematics may play a role in the COT of these groups. To examine this proximate mechanism, we digitally measured hip angle while standing (top of scapula to hock; Table S1) from lateral-view photographs of the study animals and American Kennel Club breed standards (www.akc.org/dog-breeds/), as well as gray wolves. Northern breeds exhibited a more upright stance, with the hindlimbs positioned closer to their CoM (mean hip angle=109.4±1.1 deg; Fig. 6B), nearly identical to that of gray wolves (mean hip angle=108.8±1.7 deg, F3,31=33.7, P=0.99; Fig. 6A). In contrast, the hindlimbs of both hounds and retrievers were distally grounded, farther from their CoM with significantly wider hip angles than observed in northern breeds (mean hip angle=121.4±1.7 and 122.2±1.2 deg, respectively; F2,27=38.6, P<0.01 for both; Fig. 6C,D). Hounds and retrievers also held their heads in more upright positions while running, relative to the comparatively flat toplines of wolves and northern breed dogs (Fig. 6E–H).

Fig. 6.

Comparative hip and topline angles of gray wolves and study dogs. (A,E) Gray wolves (N=5), (B,F) northern breed dogs represented by an Alaskan malamute (N=15), (C,G) hounds (N=5) and (D,H) retrievers (N=10). Hip angles (A–D) were approximated from the top of the scapula to the hip's iliac crest to the hindlimb hock. Canid outlines from www.clipartof.com. Topline angles (E–H) are approximated as the obtuse angle from the flat of the back to the back of the head, with hounds and retrievers running with their heads in more upright positions than observed in wolves or northern breed dogs.

Fig. 6.

Comparative hip and topline angles of gray wolves and study dogs. (A,E) Gray wolves (N=5), (B,F) northern breed dogs represented by an Alaskan malamute (N=15), (C,G) hounds (N=5) and (D,H) retrievers (N=10). Hip angles (A–D) were approximated from the top of the scapula to the hip's iliac crest to the hindlimb hock. Canid outlines from www.clipartof.com. Topline angles (E–H) are approximated as the obtuse angle from the flat of the back to the back of the head, with hounds and retrievers running with their heads in more upright positions than observed in wolves or northern breed dogs.

Although this is a preliminary assessment, there are several mechanical advantages of the upright stance and flat topline of northern breed dogs and wolves that could impact the energetic costs of running. By aligning the joints and segments of the hindlimbs more closely with the ground reaction force vector exerted at the foot (Gray, 1968), the more proximal and erect orientation of northern breed hindlimbs reduces excessive bone and muscle stress (Biewener, 1989). It also provides an effective mechanical advantage for loading the tendons of the leg muscles and ligaments of the foot (Alexander and Ker, 1990; Biewener, 1989, 1998; Reilly et al., 2007), likely contributing to the relative locomotor economy observed in northern breeds. These connective tissues function like ‘springy struts’ (Wentink, 1979) or pogo sticks to temporarily store, then return, the elastic strain energy necessary to move the limb and body (reviewed in Alexander, 1990, 2002; Blickhan, 1989; Ker, 1981; Taylor, 1994) and are especially important during trotting (Cavagna et al., 1977; Gregersen et al., 1998).

Several studies have investigated the muscle–tendon architecture of the canid hindlimb (Shahar and Milgram, 2001) and its effect on speed and power generation (Kemp et al., 2005; Pasi and Carrier, 2003; Williams et al., 2008), but the role of comparative functional anatomy in promoting locomotor economy across dog breeds and canids in general remains largely unexplored. Here, we speculate that specialized tendon loading and energy recovery may provide a natural mechanism enabling wolves and other large canids to track prey over long distances (e.g. Mech et al., 2015; Sheldon, 1992). When retained through domestication, such a mechanism may help explain the exceptional physiological performance of northern breed dogs during extreme distance events such as the 1600 km Iditarod Trail race and other endurance trials (Gerth et al., 2010; Hinchcliff et al., 1997; Miller et al., 2014; Van Citters and Franklin, 1969).

Acknowledgements

We thank J. Estes, C. C. Wilmers, P. Raimondi and members of the T. M. Williams lab for their editorial support, all dog owners, as well as D. Sur, C. Hill, C. Casey, C. Reichmuth, T. Kendall and B. Richter for dog handling and training assistance.

Footnotes

Author contributions

C.M.B. and T.M.W. conceived and designed the study. C.M.B. and T.M.W. conducted all experiments. C.M.B. analyzed the data and wrote the manuscript with editorial advice provided by T.M.W.

Funding

Support was provided by the National Science Foundation (DBI 0963022, DBI 1255913, GK-12 DGE-0947923), with additional support from several small grants to C.M.B. from the Science Internship Program (SIP) and the Ecology and Evolutionary Biology (EEB) Department at University of California, Santa Cruz.

References

Alexander
,
R. M. N.
(
1984
).
The gaits of bipedal and quadrupedal animals
.
Int. J. Rob. Res.
3
,
49
-
59
.
Alexander
,
R. M. N.
(
1988
).
Elastic Mechanisms in Animal Movement
.
Cambridge
,
England
:
Cambridge University Press
.
Alexander
,
R. M. N.
(
1990
).
Three uses for springs in legged locomotion
.
Int. J. Rob. Res.
9
,
53
-
61
.
Alexander
,
R. M. N.
(
2001
).
Damper for bad vibrations
.
Nature
414
,
855
-
857
.
Alexander
,
R. M. N.
(
2002
).
Tendon elasticity and muscle function
.
Comp. Biochem. Physiol. A Mol. Integr. Physiol.
133
,
1001
-
1011
.
Alexander
,
R. M. N.
(
2005
).
Models and the scaling of energy costs for locomotion
.
J. Exp. Biol.
208
,
1645
-
1652
.
Alexander
,
R. M. N.
and
Jayes
,
A. S.
(
1983
).
A dynamic similarity hypothesis for the gaits of quadrupedal mammals
.
J. Zool.
201
,
135
-
152
.
Alexander
,
R. M. N.
and
Ker
,
R. F.
(
1990
).
Running is priced by the step
.
Nature
346
,
220
-
221
.
American Kennel Club
(
2006
).
The Complete Dog Book
, 20th edn.
New York
:
Ballantine Books
.
Bennett
,
A. F.
and
Ruben
,
J. A.
(
1979
).
Endothermy and activity in vertebrates
.
Science
206
,
649
-
654
.
Bermingham
,
E. N.
,
Thomas
,
D. G.
,
Cave
,
N. J.
,
Morris
,
P. J.
,
Butterwick
,
R. F.
and
German
,
A. J.
(
2014
).
Energy requirements of adult dogs: a meta-analysis
.
PLoS ONE
9
,
e109681
.
Biewener
,
A. A.
(
1989
).
Scaling body support in mammals: limb posture and muscle mechanics
.
Science
245
,
45
-
48
.
Biewener
,
A. A.
(
1990
).
Biomechanics of mammalian terrestrial locomotion
.
Science
250
,
1097
-
1103
.
Biewener
,
A. A.
(
1998
).
Muscle-tendon stresses and elastic energy storage during locomotion in the horse
.
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
120
,
73
-
87
.
Biewener
,
A. A.
(
2006
).
Patterns of mechanical energy change in tetrapod gait: pendula, springs and work
.
J. Exp. Zool. A Comp. Exp. Biol.
305A
,
899
-
911
.
Blickhan
,
R.
(
1989
).
The spring-mass model for running and hopping
.
J. Biomech.
22
,
1217
-
1227
.
Boisclair
,
D.
and
Leggett
,
W. C.
(
1989
).
The importance of activity in bioenergetics models applied to actively foraging fishes
.
Can. J. Fish. Aquat. Sci.
46
,
1859
-
1867
.
Brown
,
J. H.
,
Gillooly
,
J. F.
,
Allen
,
A. P.
,
Savage
,
V. M.
and
West
,
G. B.
(
2004
).
Toward a metabolic theory of ecology
.
Ecology
85
,
1771
-
1789
.
Carbone
,
C.
,
Teacher
,
A.
and
Rowcliffe
,
J. M.
(
2007
).
The costs of carnivory
.
PLoS Biol.
5
,
363
-
368
.
Carbone
,
C.
,
Pettorelli
,
N.
and
Stephens
,
P. A.
(
2011
).
The bigger they come, the harder they fall: body size and prey abundance influence predator-prey ratios
.
Biol. Lett.
7
,
312
-
315
.
Careau
,
V.
,
Réale
,
D.
,
Humphries
,
M. M.
and
Thomas
,
D. W.
(
2010
).
The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs
.
Am. Nat.
175
,
753
-
758
.
Cavagna
,
G. A.
and
Kaneko
,
M.
(
1977
).
Mechanical work and efficiency in level walking and running
.
J. Physiol.
268
,
467
-
481
.
Cavagna
,
G. A.
,
Heglund
,
N. C.
and
Taylor
,
C. R.
(
1977
).
Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure
.
Am. J. Physiol.
233
,
R2430-RR261
.
Cavagna
,
G. A.
,
Franzetti
,
P.
,
Heglund
,
N. C.
and
Willems
,
P.
(
1988
).
The determinants of the step frequency in running, trotting and hopping in man and other vertebrates
.
J. Physiol.
81
-
92
.
Clutton-Brock
,
J.
(
1999
).
A Natural History of Domesticated Mammals
, 2nd edn.
Cambridge
:
Cambridge University Press
.
Drake
,
A. G.
,
Coquerelle
,
M.
and
Colombeau
,
G.
(
2015
).
3D morphometric analysis of fossil canid skulls contradicts the suggested domestication of dogs during the late Paleolithic
.
Nat. Sci. Rep.
5
,
1
-
8
.
Fedak
,
M. A.
,
Rome
,
L.
and
Seeherman
,
H. J.
(
1981
).
One-step N2-dilution technique for calibrating open-circuit VO2 measuring systems
.
J. Appl. Physiol.
51
,
772
-
776
.
Fischer
,
M. S.
and
Lilje
,
K. E.
(
2011
).
Dogs in Motion
.
London
:
The Pet Book Publishing Company
.
Freedman
,
A. H.
,
Gronau
,
I.
,
Schweizer
,
R. M.
,
Ortega-Del Vecchyo
,
D.
,
Han
,
E.
,
Silva
,
P. M.
,
Galaverni
,
M.
,
Fan
,
Z.
,
Marx
,
P.
,
Lorente-Galdos
,
B.
, et al. 
(
2014
).
Genome sequencing highlights the dynamic early history of dogs
.
PLoS Genet.
10
,
e1004016
.
Galibert
,
F.
,
Quignon
,
P.
,
Hitte
,
C.
and
André
,
C.
(
2011
).
Toward understanding dog evolutionary and domestication history
.
Comptes Rendus Biol.
334
,
190
-
196
.
Garland
,
T. J.
(
1983
).
Scaling the ecological cost of transport to body mass in terrestrial mammals
.
Am. Nat.
121
,
571
-
587
.
Gerth
,
N.
,
Redman
,
P.
,
Speakman
,
J.
,
Jackson
,
S.
and
Starck
,
J. M.
(
2010
).
Energy metabolism of Inuit sled dogs
.
J. Comp. Physiol. B Biochem. Syst. Environ. Physiol.
180
,
577
-
589
.
Girard
,
I.
(
2001
).
Field cost of activity in the kit fox, Vulpes macrotis
.
Physiol. Biochem. Zool.
74
,
191
-
202
.
Gomeñuka
,
N. A.
,
Bona
,
R. L.
,
da Rosa
,
R. G.
and
Peyré-Tartaruga
,
L. A.
(
2014
).
Adaptations to changing speed, load, and gradient in human walking: cost of transport, optimal speed, and pendulum
.
Scand. J. Med. Sci. Sports
24
,
e165
-
e173
.
Gomeñuka
,
N. A.
,
Bona
,
R. L.
,
da Rosa
,
R. G.
and
Peyré-Tartaruga
,
L. A.
(
2016
).
The pendular mechanism does not determine the optimal speed of loaded walking on gradients
.
Hum. Mov. Sci.
47
,
175
-
185
.
Gorman
,
M. L.
,
Mills
,
M. G.
,
Raath
,
J. P.
and
Speakman
,
J. R.
(
1998
).
High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas
.
Nature
391
,
479
-
481
.
Gray
,
J.
(
1968
).
Animal Locomotion
.
New York
:
W.W. Norton & Company, Inc
.
Gregersen
,
C. S.
,
Silverton
,
N. A.
and
Carrier
,
D. R.
(
1998
).
External work and potential for elastic storage at the limb joints of running dogs
.
J. Exp. Biol.
201
,
3197
-
3210
.
Griffin
,
T. M.
,
Main
,
R. P.
and
Farley
,
C. T.
(
2004
).
Biomechanics of quadrupedal walking: how do four-legged animals achieve inverted pendulum-like movements?
J. Exp. Biol.
207
,
3545
-
3558
.
Halsey
,
L. G.
(
2011
).
The challenge of measuring energy expenditure: current field and laboratory methods
.
Comp. Biochem. Physiol. A Mol. Integr. Physiol.
158
,
247
-
251
.
Halsey
,
L. G.
(
2013
).
The relationship between energy expenditure and speed during pedestrian locomotion in birds: a morphological basis for the elevated y-intercept?
Comp. Biochem. Physiol. A Mol. Integr. Physiol.
165
,
295
-
298
.
Halsey
,
L. G.
(
2016
).
Terrestrial movement energetics: current knowledge and its application to the optimising animal
.
J. Exp. Biol.
219
,
1424
-
1431
.
Hammond
,
K. A.
,
Konarzewski
,
M.
,
Torres
,
R. M.
and
Diamond
,
J.
(
1994
).
Metabolic ceilings under a combination of peak energy demands
.
Physiol. Zool.
67
,
1479
-
1506
.
Heglund
,
N. C.
and
Taylor
,
C. R.
(
1988
).
Speed, stride frequency and energy cost per stride: how do they change with body size and gait?
J. Exp. Biol.
138
,
301
-
318
.
Hermanson
,
J. W.
(
1997
).
Architecture and the division of labor in the extensor carpi radialis muscle of horses
.
Acta Anat.
159
,
127
-
135
.
Hinchcliff
,
K. W.
,
Reinhart
,
G. A.
,
Burr
,
J. R.
,
Schreier
,
C. J.
and
Swenson
,
R. A.
(
1997
).
Metabolizable energy intake and sustained energy expenditure of Alaskan sled dogs during heavy exertion in the cold
.
Am. J. Vet. Res.
58
,
1457
-
1462
.
Hoyt
,
D. F.
and
Taylor
,
C. R.
(
1981
).
Gait and the energetics of locomotion in horses
.
Nature
292
,
239
-
240
.
Hoyt
,
D. F.
,
Wickler
,
S. J.
and
Cogger
,
E. A.
(
2000
).
Time of contact and step length: the effect of limb length, running speed, load carrying and incline
.
J. Exp. Biol.
203
,
221
-
227
.
Hoyt
,
D. F.
,
Wickler
,
S. J.
,
Dutto
,
D. J.
,
Catterfeld
,
G. E.
and
Johnsen
,
D.
(
2006
).
What are the relations between mechanics, gait parameters, and energetics in terrestrial locomotion?
J. Exp. Zool. A Comp. Exp. Biol.
305A
,
912
-
922
.
Huson
,
H. J.
,
Parker
,
H. G.
,
Runstadler
,
J.
and
Ostrander
,
E. A.
(
2010
).
A genetic dissection of breed composition and performance enhancement in the Alaskan sled dog
.
BMC Genet.
11
,
71
.
Jayes
,
A. S.
and
Alexander
,
R. M. N.
(
1978
).
Mechanics of locomotion of dogs (Canis familiaris) and sheep (Ovis aries)
.
J. Zool.
185
,
289
-
308
.
Jimenez
,
A. G.
(
2016
).
Physiological underpinnings in life-history trade-offs in man's most popular selection experiment: the dog
.
J. Comp. Physiol. B Biochem. Syst. Environ. Physiol.
186
,
813
-
827
.
Kar
,
D. C.
,
Kurien Issac
,
K.
and
Jayarajan
,
K.
(
2003
).
Gaits and energetics in terrestrial legged locomotion
.
Mech. Mach. Theory
38
,
355
-
366
.
Karasov
,
W. H.
(
1992
).
Daily energy expenditure and the cost of activity in mammals
.
Am. Zool.
32
,
238
-
248
.
Kemp
,
T. J.
,
Bachus
,
K. N.
,
Nairn
,
J. A.
and
Carrier
,
D. R.
(
2005
).
Functional trade-offs in the limb bones of dogs selected for running versus fighting
.
J. Exp. Biol.
208
,
3475
-
3482
.
Ker
,
R. F.
(
1981
).
Dynamic tensile properties of the plantaris tendon of sheep (Ovis aries)
.
J. Exp. Biol.
93
,
283
-
302
.
Kleiman
,
D. G.
,
Geist
,
V.
and
McDade
,
M. C.
eds. (
2003
).
Grzimek's Animal Life Encyclopedia: Mammals
. 2nd edn.
Gale
.
Koteja
,
P.
(
1987
).
On the relation between basal and maximum metabolic rate in mammals
.
Comp. Biochem. Physiol. A. Comp. Physiol.
87
,
205
-
208
.
Kram
,
R.
and
Taylor
,
C. R.
(
1990
).
Energetics of running: a new perspective
.
Nature
346
,
265
-
267
.
Larson
,
G.
,
Karlsson
,
E. K.
,
Perri
,
A.
,
Webster
,
M. T.
,
Ho
,
S. Y. W.
,
Peters
,
J.
,
Stahl
,
P. W.
,
Piper
,
P. J.
,
Lingaas
,
F.
,
Fredholm
,
M.
, et al. 
(
2012
).
Rethinking dog domestication by integrating genetics, archeology, and biogeography
.
Proc. Natl. Acad. Sci. USA
109
,
8878
-
8883
.
Lewis
,
L. D.
(
1995
).
Equine Clinical Nutrition: Feeding and Care
.
Oxford
:
Wiley-Blackwell
.
Lindblad-Toh
,
K.
,
Wade
,
C. M.
,
Mikkelsen
,
T. S.
,
Karlsson
,
E. K.
,
Jaffe
,
D. B.
,
Kamal
,
M.
,
Clamp
,
M.
,
Chang
,
J. L.
,
Kulbokas
,
E. J.
,
Zody
,
M. C.
, et al. 
(
2005
).
Genome sequence, comparative analysis and haplotype structure of the domestic dog
.
Nature
438
,
803
-
819
.
Maes
,
L. D.
,
Herbin
,
M.
,
Hackert
,
R.
,
Bels
,
V. L.
and
Abourachid
,
A.
(
2008
).
Steady locomotion in dogs: temporal and associated spatial coordination patterns and the effect of speed
.
J. Exp. Biol.
211
,
138
-
149
.
Mech
,
L. D.
(
1970
).
The Wolf: The Behavior and Ecology of an Endangered Species
.
New York
:
Natural History Press
.
Mech
,
L. D.
(
1994
).
Regular and homeward travel speeds of Arctic wolves
.
J. Mammal.
75
,
741
-
742
.
Mech
,
L. D.
and
Cluff
,
H. D.
(
2011
).
Movements of wolves at the northern extreme of the species’ range, including during four months of darkness
.
PLoS ONE
6
,
2
-
6
.
Mech
,
L. D.
,
Smith
,
D. W.
and
MacNulty
,
D. R.
(
2015
).
Introduction: the wolf as a killing machine
. In
Wolves On the Hunt: The Behavior of Wolves Hunting Wild Prey
.
Chicago
:
University of Chicago Press
.
Miller
,
B. F.
,
Drake
,
J. C.
,
Peelor
,
F. F.
,
Biela
,
L. M.
,
Geor
,
R. J.
,
Hinchcliff
,
K. W.
,
Davis
,
M.
and
Hamilton
,
K. L.
(
2014
).
Participation in a 1000-mile race increases the oxidation of carbohydrate in Alaskan sled dogs
.
J. Appl. Physiol.
118
,
1502
-
1509
.
Miller
,
B. F.
,
Ehrlicher
,
S. E.
,
Drake
,
J. C.
,
Peelor
,
F. F.
,
Biela
,
L. M.
,
Pratt-Phillips
,
S.
,
Davis
,
M.
,
Hamilton
,
K. L.
,
Frederick
,
F.
,
Biela
,
L. M.
, et al. 
(
2015
).
Assessment of protein synthesis in highly aerobic canine species at the onset and during exercise training
.
J. Appl. Physiol.
118
,
811
-
817
.
Nanua
,
P.
and
Waldron
,
K. J.
(
1995
).
Energy comparison between trot, bound, and gallop using a simple model
.
J. Biomech. Eng.
117
,
466
-
473
.
National Research Council
(
2006
).
Nutrient Requirements of Dogs and Cats
.
Washington, DC
:
National Academies Press
.
Okarma
,
H.
and
Koteja
,
P.
(
1987
).
Metabolic rate in the gray wolf in Poland
.
J. Wildl. Manage.
51
,
800
-
801
.
Packard
,
G. C.
and
Boardman
,
T. J.
(
1999
).
The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort?
Comp. Biochem. Physiol. A Mol. Integr. Physiol.
122
,
37
-
44
.
Pagan
,
J. D.
and
Hintz
,
H. F.
(
1986
).
Energy expenditure in horses during submaximal exercise
.
J. Anim. Sci.
63
,
822
-
830
.
Parker
,
H. G.
(
2012
).
Genomic analyses of modern dog breeds
.
Mamm. Genome
23
,
19
-
27
.
Parker
,
H. G.
,
Kim
,
L. V.
,
Sutter
,
N. B.
,
Carlson
,
S.
,
Lorentzen
,
T. D.
,
Malek
,
T. B.
,
Johnson
,
G. S.
,
DeFrance
,
H. B.
,
Ostrander
,
E. A.
and
Kruglyak
,
L.
(
2004
).
Genetic structure of the purebred domestic dog
.
Science
304
,
1160
-
1164
.
Pasi
,
B. M.
and
Carrier
,
D. R.
(
2003
).
Functional trade-offs in the limb muscles of dogs selected for running vs. fighting
.
J. Evol. Biol.
16
,
324
-
332
.
Perri
,
A.
(
2016
).
A wolf in dog's clothing: initial dog domestication and Pleistocene wolf variation
.
J. Archaeol. Sci.
68
,
1
-
4
.
Perry
,
A. K.
,
Blickhan
,
R.
,
Biewener
,
A. A.
,
Heglund
,
N. C.
and
Taylor
,
C. R.
(
1988
).
Preferred speeds in terrestrial vertebrates: are they equivalent?
J. Exp. Biol.
137
,
207
-
219
.
Peters
,
R. H.
(
1983
).
The Ecological Implications of Body Size
.
Cambridge
:
Cambridge University Press
.
Pionnier-Capitan
,
M.
,
Bemilli
,
C.
,
Bodu
,
P.
,
Célérier
,
G.
,
Ferrié
,
J.-G.
,
Fosse
,
P.
,
Garcià
,
M.
and
Vigne
,
J.-D.
(
2011
).
New evidence for Upper Palaeolithic small domestic dogs in South-Western Europe
.
J. Archaeol. Sci.
38
,
2123
-
2140
.
Pontzer
,
H.
(
2016
).
A unified theory for the energy cost of legged locomotion
.
Biol. Lett.
12
,
20150935
.
Poole
,
D. C.
and
Erickson
,
H. H.
(
2011
).
Highly athletic terrestrial mammals: horses and dogs
.
Compr. Physiol.
1
,
1
-
37
.
Raab
,
J. L.
,
Eng
,
P.
and
Waschler
,
R. A.
(
1976
).
Metabolic cost of grade running in dogs
.
J. Appl. Physiol.
41
,
532
-
535
.
Reilly
,
S. M.
,
McElroy
,
E. J.
and
Biknevicius
,
A. R.
(
2007
).
Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods
.
Zoology
110
,
271
-
289
.
Rennick
,
P.
ed. (
1987
).
Dogs of the North
.
Anchorage, AK
:
Alaska Geographic Society
.
Rezende
,
E. L.
,
Gomes
,
F. R.
,
Chappell
,
M. A.
and
Garland
,
T.
, Jr
. (
2009
).
Running behavior and its energy cost in mice selectively bred for high voluntary locomotor activity
.
Physiol. Biochem. Zool.
82
,
662
-
679
.
Scantlebury
,
D. M.
,
Mills
,
M. G. L.
,
Wilson
,
R. P.
,
Wilson
,
J. W.
,
Mills
,
M. E. J.
,
Durant
,
S. M.
,
Bennett
,
N. C.
,
Bradford
,
P.
,
Marks
,
N. J.
and
Speakman
,
J. R.
(
2014
).
Flexible energetics of cheetah hunting strategies provide resistance against kleptoparasitism
.
Science
346
,
79
-
81
.
Schmidt-Nielsen
,
K.
(
1972
).
Locomotion: energy cost of swimming, flying, and running
.
Science
177
,
222
-
228
.
Schmidt-Nielsen
,
K.
(
1997
).
Animal Physiology: Adaptation and Environment
, 5th edn.
New York
:
Cambridge University Press
.
Seeherman
,
H. J.
,
Taylor
,
C. R.
,
Maloiy
,
G. M. O.
and
Armstrong
,
R. B.
(
1981
).
Design of the mammalian respiratory system. II. Measuring maximum aerobic capacity
.
Respir. Physiol.
44
,
11
-
23
.
Shahar
,
R.
and
Milgram
,
J.
(
2001
).
Morphometric and anatomic study of the hind limb of a dog
.
Am. J. Vet. Res.
62
,
928
-
933
.
Sheldon
,
J. W.
(
1992
).
Wild Dogs: The Natural History of the Nondomesticated Canidae
.
San Diego
:
Academic Press
.
Skoglund
,
P.
,
Ersmark
,
E.
,
Palkopoulou
,
E.
and
Dalén
,
L.
(
2015
).
Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds
.
Curr. Biol.
25
,
1515
-
1519
.
Snow
,
D. H.
(
1985
).
The horse and dog, elite athletes—why and how?
Proc. Nutr. Soc.
44
,
267
-
272
.
Speakman
,
J. R.
,
Van Acker
,
A.
and
Harper
,
E. J.
(
2003
).
Age-related changes in the metabolism and body composition of three dog breeds and their relationship to life expectancy
.
Aging Cell
2
,
265
-
275
.
Tatner
,
P.
and
Bryant
,
D. M.
(
1986
).
Flight cost of a small passerine measured using doubly labeled water: implications for energetics studies
.
Auk
103
,
169
-
180
.
Taylor
,
C. R.
(
1994
).
Relating mechanics and energetics during exercise
.
Adv. Vet. Sci. Comp. Med.
38A
,
181
-
215
.
Taylor
,
C. R.
,
Heglund
,
N. C.
and
Maloiy
,
G. M.
(
1982
).
Energetics and mechanics of terrestrial locomotion 1. Metabolic energy consumption as a function of speed and body size in birds and mammals
.
J. Exp. Biol.
97
,
1
-
21
.
Taylor
,
C. R.
,
Karas
,
R. H.
,
Weibel
,
E. R.
and
Hoppeler
,
H.
(
1987a
).
Adaptive variation in the mammalian respiratory system in relation to energetic demand: II. Reaching the limits to oxygen flow
.
Respir. Physiol.
69
,
7
-
26
.
Taylor
,
C. R.
,
Weibel
,
E. R.
,
Karas
,
R. H.
and
Hoppeler
,
H.
(
1987b
).
Adaptive variation in the mammalian respiratory system in relation to energetic demand: VIII. Structural and functional design principles determining the limits to oxidative metabolism
.
Respir. Physiol.
69
,
117
-
127
.
Torres
,
B. T.
,
Moëns
,
N. M. M.
,
Al-Nadaf
,
S.
,
Reynolds
,
L. R.
,
Fu
,
Y.-C.
and
Budsberg
,
S. C.
(
2013
).
Comparison of overground and treadmill based gaits of dogs
.
Am. J. Vet. Res.
74
,
535
-
541
.
Udell
,
M. A. R.
,
Dorey
,
N. R.
and
Wynne
,
C. D. L.
(
2010
).
What did domestication do to dogs? A new account of dogs’ sensitivity to human actions
.
Biol. Rev.
85
,
327
-
345
.
Van Citters
,
R. L.
and
Franklin
,
D. L.
(
1969
).
Cardiovascular performance of Alaska sled dogs during exercise
.
Circ. Res.
24
,
33
-
42
.
Vaysse
,
A.
,
Ratnakumar
,
A.
,
Derrien
,
T.
,
Axelsson
,
E.
,
Rosengren Pielberg
,
G.
,
Sigurdsson
,
S.
,
Fall
,
T.
,
Seppälä
,
E. H.
,
Hansen
,
M. S. T.
,
Lawley
,
C. T.
, et al. 
(
2011
).
Identification of genomic regions associated with phenotypic variation between dog breeds using selection mapping
.
PLoS Genet.
7
,
e1002316
.
VonHoldt
,
B. M.
,
Pollinger
,
J. P.
,
Lohmueller
,
K. E.
,
Han
,
E.
,
Parker
,
H. G.
,
Quignon
,
P.
,
Degenhardt
,
J. D.
,
Boyko
,
A. R.
,
Earl
,
D. A.
,
Auton
,
A.
, et al. 
(
2010
).
Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication
.
Nature
464
,
898
-
902
.
Wang
,
G.-D.
,
Zhai
,
W.
,
Yang
,
H.-C.
,
Fan
,
R.-X.
,
Cao
,
X.
,
Zhong
,
L.
,
Wang
,
L.
,
Liu
,
F.
,
Wu
,
H.
,
Cheng
,
L.-G.
, et al. 
(
2013
).
The genomics of selection in dogs and the parallel evolution between dogs and humans
.
Nat. Commun.
4
,
1860
.
Wang
,
G.-D.
,
Zhai
,
W.
,
Yang
,
H.-C.
,
Wang
,
L.
,
Zhong
,
L.
,
Liu
,
Y.-H.
,
Fan
,
R.-X.
,
Yin
,
T.-T.
,
Zhu
,
C.-L.
,
Poyarkov
,
A. D.
, et al. 
(
2016
).
Out of southern East Asia: the natural history of domestic dogs across the world
.
Cell Res.
26
,
21
-
33
.
Wayne
,
R. K.
(
1986
).
Limb morphology of domestic and wild canids: the influence of development on morphologic change
.
J. Morphol.
187
,
301
-
319
.
Wayne
,
R. K.
(
2001
).
Consequences of domestication: morphological diversity of the dog
. In
The Genetics of the Dog
(ed.
A.
Ruvinksy
and
J.
Sampson
.), pp.
43
-
60
.
Oxon
,
UK
:
CABI Publishing
.
Weibel
,
E. R.
and
Hoppeler
,
H.
(
2005
).
Exercise-induced maximal metabolic rate scales with muscle aerobic capacity
.
J. Exp. Biol.
208
,
1635
-
1644
.
Weibel
,
E. R.
,
Taylor
,
C. R.
,
Neil
,
J. J. O.
,
Leith
,
D. E.
,
Gehr
,
P.
,
Hoppeler
,
H.
,
Langman
,
V.
and
Baudinette
,
R. V.
(
1983
).
Maximal oxygen consumption and pulmonary diffusing capacity: a direct comparison of physiologic and morphometric measurements in canids
.
Respir. Physiol.
54
,
173
-
188
.
Weibel
,
E. R.
,
Taylor
,
C. R.
,
Hoppeler
,
H.
and
Karas
,
R. H.
(
1987
).
Adaptive variation in the mammalian respiratory system in relation to energetic demand: I: introduction to problem and strategy
.
Respir. Physiol.
69
,
1
-
6
.
Weibel
,
E. R.
,
Bacigalupe
,
L. D.
,
Schmitt
,
B.
and
Hoppeler
,
H.
(
2004
).
Allometric scaling of maximal metabolic rate in mammals: muscle aerobic capacity as determinant factor
.
Respir. Physiol. Neurobiol.
140
,
115
-
132
.
Wentink
,
G. H.
(
1979
).
Dynamics of the hind limb at walk in horse and dog
.
Anat. Embryol.
155
,
179
-
190
.
Westerterp
,
K.
,
Saris
,
W.
,
Van Es
,
M.
and
ten Hoor
,
F.
(
1986
).
Use of the doubly labeled water technique in humans during heavy sustained exercise
.
J. Appl. Physiol.
61
,
2161
-
2167
.
Wilcox
,
B.
and
Walkowicz
,
C.
(
1995
).
Atlas of Dog Breeds of the World
, 5th edn.
Neptune City, NJ
:
T.F.H. Publications
.
Williams
,
T. M.
(
1999
).
The evolution of cost efficient swimming in marine mammals: limits to energetic optimization
.
Philos. Trans. R. Soc. Lond. B. Biol. Sci.
354
,
193
-
201
.
Williams
,
T. M.
,
Ben-David
,
M.
,
Noren
,
S.
,
Rutishauser
,
M.
,
McDonald
,
K.
and
Heyward
,
W.
(
2002
).
Running energetics of the North American river otter: do short legs necessarily reduce efficiency on land?
Comp. Biochem. Physiol. A. Mol. Integr. Physiol.
133
,
203
-
212
.
Williams
,
S. B.
,
Wilson
,
A. M.
,
Rhodes
,
L.
,
Andrews
,
J.
and
Payne
,
R. C.
(
2008
).
Functional anatomy and muscle moment arms of the pelvic limb of an elite sprinting athlete: the racing greyhound (Canis familiaris)
.
J. Anat.
213
,
361
-
372
.
Wilson
,
A. M.
,
van den Borget
,
A. J.
and
McGuigan
,
M. P.
(
2000
).
Optimization of the muscle-tendon unit for economical locomotion in cursorial animals
. In
Skeletal Muscle Mechanics: From Mechanisms to Function
(ed.
W.
Herzog
), pp.
517
-
547
.
New York
:
Wiley
.
Wilson
,
A. M.
,
McGuigan
,
M. P.
,
Su
,
A.
and
van Den Bogert
,
A. J.
(
2001
).
Horses damp the spring in their step
.
Nature
414
,
895
-
899
.
Withers
,
C.
(
1977
).
Measurement of VO2, VCO2, and evaporative water loss with a flow-through mask
.
J. Appl. Physiol.
42
,
120
-
123
.

Competing interests

The authors declare no competing or financial interests.

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