RESEARCH ARTICLE

Ontogenetic Change of the Weight Support Pattern in Growing Dogs DANIELA HELMSMÜLLER1, ALEXANDRA ANDERS1, INGO NOLTE1, 2 AND NADJA SCHILLING * 1

Small Animal Clinic, University of Veterinary Medicine Hannover, Foundation, Hannover, Germany Institute of Systematic Zoology and Evolutionary Biology, Friedrich‐Schiller‐University, Jena, Germany

2

ABSTRACT

J. Exp. Zool. 321A:254–264, 2014

Weight support patterns vary widely among mammals. Differences in how much of the body weight is supported by the fore‐ versus the hind‐limbs are well documented among and within species. Intraindividual variation due to ontogenetic processes has been studied in several hindlimb‐ dominated species and consistently showed a caudal shift in the limbs' support roles. We hypothesized that forelimb‐dominated species exhibit a cranial shift in their support pattern and tested this hypothesis by examining the vertical ground reaction forces in growing dogs. Six male Beagle siblings were studied from 9 to 51 postnatal weeks (PW) of age while they trotted on an instrumented treadmill. Ontogenetic shifting in fore‐to‐hind support was evaluated using vertical force ratios (i.e., peak and impulse) as well as the stance time ratio of the fore‐ and the hind‐limbs. Because morphological and kinematic characteristics influence weight support patterns, changes in body shape (i.e., trunk shape), and average limb position were determined. As in adult dogs, the forelimbs carried a greater proportion of the body weight than the hindlimbs at all ages. When the dogs were younger, peak vertical force occurred earlier during stance in the hindlimbs but not the forelimbs. Both the increasing ratio of the vertical force and the increasing ratio of the stance times indicate an increasing weight support by the forelimbs (i.e., 59% at PW9 vs. 63% at PW51). The observed ontogenetic changes in trunk shape and average limb angle were consistent with this cranial shift in weight support. J. Exp. Zool. 321A:254–264, 2014. © 2014 Wiley Periodicals, Inc. How to cite this article: Helmsmüller D, Anders A, Nolte I, Schilling N. 2014. Ontogenetic change of the weight support pattern in growing dogs. J. Exp. Zool. 321A:254–264.

The role that fore‐ and hindlimbs play in supporting the body's weight during locomotion varies among quadrupedal mammals. It is well‐documented, for example, that primates support a greater proportion of their body weight (BW) with their hindlimbs, while most other mammals bear more weight on their forelimbs (e.g., Krüger, '43; Kimura, '92; Demes et al., '94). Among non‐primate mammals, species with massive forelimbs and/or heads carry a greater proportion of their BW on the forelimbs compared to species with rather muscular hindlimbs (e.g., dromedary: 62% forelimb support vs. cheetah: 52%; Krüger, '43). Intraspecific variation in the fore‐to‐hind BW distribution has also been observed among breeds with different builds (e.g., Krüger, '43; Back et al., 2007). Dogs selected for high acceleration and speed (i.e., with large hindlimb muscles; Pasi and Carrier, 2003; Williams et al., 2008) support a smaller proportion of their BW with the

Grant sponsor: Friedrich‐Schiller‐University Jena; grant sponsor: Berufsgenossenschaft Nahrungsmittel und Gastgewerbe (Erfurt); grant sponsor: Hannoversche Gesellschaft zur Förderung der Kleintiermedizin (HGFK). Conflicts of interest: None. This study represents a part of the Doctoral thesis by D.H. as partial fulfillment of the requirements for a Dr. med. vet. degree.  Correspondence to: Nadja Schilling, Friedrich‐Schiller‐Universität, Institut für Spezielle Zoologie und Evolutionsbiologie, Erbertstr. 1, 07743 Jena, Germany. E‐mail: [email protected] Received 11 April 2013; Revised 24 December 2013; Accepted 18 January 2014 DOI: 10.1002/jez.1856 Published online 14 February 2014 in Wiley Online Library (wileyonlinelibrary.com).

© 2014 WILEY PERIODICALS, INC.

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WEIGHT SUPPORT SHIFT IN GROWING DOGS forelimbs than breeds with more muscular chests and large heads (e.g., Barzoi 57% vs. Rottweiler 64%; Bertram et al., 2000; Voss et al., 2011). Various hypotheses have been proposed to explain differences in the support patterns (Gray, '44; Reynolds, '85a). “Passive models” suggest anatomical features (i.e., variation in the anterior–posterior distribution of body mass) to account for the fore‐to‐hind support asymmetries. In “active models,” the animal alters the limbs' support roles by adjusting average limb position (e.g., displaying more or less retracted limbs and thus changing the position of the feet relative to the body's center of mass, CoM) or by changing muscular activity (e.g., limb retractor recruitment). Support for these hypotheses comes from morphological, kinematic, kinetic, or electromyographic studies (e.g., Rollinson and Martin, '81; Demes et al., '94; Grand, '97; Larson et al., 2001; Young et al., 2007; Larson and Stern, 2009) but whether or not all of these features contribute to the pattern observed in a given species has been discussed controversially (e.g., Raichlen et al., 2009; Larson and Demes, 2011). The studies mentioned above focused on inter‐ and intra‐ specific differences and therefore compared fore‐to‐hind asymmetries in weight support among adults. Fewer studies investigated intraindividual variation such as the effect that ontogenetic changes have on the support roles of the limbs. Mammalian juveniles have relatively large heads compared with adults (e.g., Trotter et al., '75; Kimura, '87; Schilling and Petrovitch, 2006; Helmsmüller et al., 2013). This together with the hindlimbs increasing in length and/or muscularity more than the forelimbs leads to a net caudal translation of the CoM and a decreasing role of the forelimbs in weight support during growth (rhesus macaque: Grand, '77; Turnquist and Wells, '94; chimpanzee: Kimura, '87; Japanese macaque: Kimura, 2000; koala: Grand and Barboza, 2001; yellow baboon: Shapiro and Raichlen, 2006; squirrel monkey: Young, 2012). Interestingly, the previous studies investigated hindlimb‐dominated species only; raising questions about whether or not an increasing role of the hindlimbs in weight support is ubiquitous for mammals and particularly species that carry more weight on their forelimbs. In order to test whether forelimb‐dominated species also show a caudal shift in their fore‐to‐hind support or whether their support pattern becomes more and more pronounced by an increasing role of the forelimbs during development, we studied the ontogenetic changes in the fore‐to‐hind weight distribution in dogs. Two observations are suggestive of an increasing forelimb role during ontogeny: first, the increasingly retracted limbs of developing non‐primate mammals (Schilling, 2005) are consistent with an increasing forelimb role in weight support. Second, mammalian juveniles often appear plump and lack the athletic body shape that their adult conspecifics show. Developing the adult appearance could be associated with a net cranial translation of the CoM in species like the dog that undergo pronounced changes in trunk shape.

Weight support roles of fore‐ versus hind‐limbs are generally determined as the ratio of the forelimbs' vertical impulse to the sum of fore‐ and hind‐limb vertical impulse (Reynolds, '85b; Raichlen et al., 2009). Therefore, we recorded the ground reaction forces (GRFs) in the dogs while trotting on an instrumented treadmill. Two parameters were tested in this longitudinal study: peak vertical force and vertical impulse. In addition, we determined the stance durations of the limbs because a higher fraction of the vertical impulse of a limb is associated with a relatively higher duty factor and the ratio between fore‐ and hind‐ limb stance times has been suggested to reflect the fore‐to‐hind support roles in trotting quadrupeds (e.g., Bertram et al., 2000; Lee et al., 2004; Witte et al., 2004). To evaluate whether the observed changes in the support patterns were associated with changes in average limb position and body shape, we collected kinematic data simultaneously with the GRF measurements and determined the change in trunk shape by calculating the ratio between the diameters of the thorax and the abdomen. In summary, the goals of this study were to determine whether the weight support pattern changes in growing dogs and, if so, to examine whether or not dogs follow the so far observed caudal shift in fore‐to‐hind weight distribution. Evaluation of average limb position and body shape allowed us to explore two of three characteristics suggested to explain differences in the support roles. Because, we did not study muscle activity, potential changes in retractor activity (“active models”) that may influence weight support cannot be evaluated.

ANIMALS AND METHODS Dogs Six male Beagle siblings (Canis lupus familiaris, Linnaeus 1758) from the same litter were used in this longitudinal study. The dogs were from a breeding colony of the University of Veterinary Medicine Hannover, Foundation (Germany) and came to the Small Animal Clinic at the age of 9 weeks (i.e., ninth postnatal week, PW9). All dogs underwent two standard orthopedic exams, one at PW14 and one at PW50, which confirmed that the dogs were healthy. The experiments were carried out in accordance with the German Animal Welfare guidelines and notice was given to the Ethics committee of Lower Saxony (Germany). Data Collection Gait analysis started at PW9, when the puppies were gently introduced to ambulating on the treadmill, and continued until PW51. Data were collected weekly up to PW20, fortnightly up to PW32 and monthly henceforth. In addition, various morphometric measurements were taken for a related study (Helmsmüller et al., 2013) and the dogs were photographed in lateral perspective standing as balanced and square as possible (Fig. 1). For the analyses, data from PW11, 13, 19, 22, 26, 30, 43, and 51 were selected. Two dogs could not participate in the data collection at J. Exp. Zool.

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HELMSMÜLLER ET AL. underneath each belt (Model 4060‐08, Bertec Corporation, Columbus, OH, USA). Because of their small body size, the puppies trotted on one side of the treadmill allowing the forces exerted by the fore‐ and the hind‐limbs to be recorded separately (sample rate 1,000 Hz). Separate force curves for left and right limbs were nevertheless obtained because the duty factor was less than 0.5 throughout. To identify whether right or left limbs exerted forces, a digital camera recorded the dogs from the lateral perspective (NVGS60, Panasonic, Germany). Two retro‐reflective markers (diameter: 9.5 mm) were attached above palpable landmarks of each limb using adhesive tape to determine average limb angle (Fig. 2). Six infrared cameras (Vicon Motion Systems Ltd., MX3þ, Oxford, UK; 100 Hz) tracked the marker positions, which represented the fulcra of the fore‐ and the hind‐limbs (i.e., proximal end of the scapular spine and hip joint indicated by the major trochanter) and the feet (i.e., proximal

Figure 1. One of the subjects at three different time points (i.e., postnatal weeks, PW) covered in this study and at a later time after the study had been finished (bottom). Size was scaled to the same trunk length to illustrate the changes in body proportions and particularly in trunk shape. The vertical lines indicate where the thoracic and abdominal diameters were measured to evaluate the change in trunk shape during the study period (i.e., between PW9 and PW51). (The two sites shaved on the back provided data for a separate study.) PW, postnatal week. PW19 and were therefore measured the following week (i.e., PW20). During data collection, the dogs trotted on a horizontal treadmill with four separate belts and integrated force plates J. Exp. Zool.

Figure 2. Determination of the average fore‐ and hind‐limb angles. A: One of the subjects with the retro‐reflective markers at the fulcra of the limbs (i.e., proximal end of the scapular spine and hip joint) and distally on the fore‐ and the hind‐feet (i.e., near the metacarpo‐ and the metatarso‐phalangeal joints, respectively). The angles between the vertical and the lines connecting the respective two limb markers at touchdown and liftoff were used to determine average limb position. B: Limb protraction (i.e., angle at touchdown) and limb retraction (i.e., angle at liftoff) were averaged to calculate average limb angle.

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WEIGHT SUPPORT SHIFT IN GROWING DOGS end of the 5th phalanx). Due to technical difficulties, the left hindlimb of two dogs at PW13 and one dog at PW22 was not detected and, therefore, sample size was then only four and five, respectively. Kinetic and kinematic data were analyzed using Vicon Nexus and Vicon Bodybuilder (Vicon Motion Systems Ltd., Oxford, UK). During each session, at least three trials per dog were obtained lasting about 30 sec and covering approximately 65 strides. Of these, 10 valid steps (i.e., without overstepping) were analyzed per dog and age. The selected strides were not always consecutive because the dogs, particularly when very young, did not run as consistently as when they were older. Touchdown and liftoff events were determined manually using the vertical force curves. To eliminate the noise intrinsic to GRF measurements obtained with instrumented treadmills (i.e., small fluctuations of the recorded force signal around zero); the force threshold was set at 5% of the dog's BW. The force data were then time‐normalized to 100% stance duration (i.e., 101 data points) using linear interpolation and exported to Microsoft Excel together with the limb angles (in °) and the temporal gait parameters (i.e., stance duration in seconds). Data Analysis Vertical force data from the 10 steps were averaged per dog and normalized to the dog's BW using equation (1): Vertical force ð%BWðsÞÞ ¼ vertical force 100=ðbody mass 9:81 m=s2 Þ ð1Þ

The vertical force parameters compared among the ages were peak force (in %BW) and vertical impulse (in %BWs). In addition, BW distribution among the four limbs, symmetry indices for the fore‐ and the hind‐limbs and time to peak vertical force (in % stance duration) were determined. BW distribution was calculated using equation (2): %BW bearing ¼ vertical force of the limb= total vertical force of all limbs 100

ð2Þ

To verify that our dogs were sound throughout the study period (i.e., limb loading was symmetrical between body sides) and ensure that the vertical force data from the fore‐ and the hind‐ limbs, respectively, could be pooled, we calculated symmetry indices (SI in %) using the following equation (according to Herzog et al., '89): SI ¼ 100% ðleft force  right forceÞ=ð0:5 ðleft force þ right forceÞÞ

ð3Þ

Thereby, the vertical forces of the left and the right limbs were averaged across the 10 steps. Perfect symmetry is given at SI ¼ 0. Deviations of up to 4% in the forelimbs and 6% in the hindlimbs are considered physiological (Budsberg et al., '93).

In addition, the ratio of the stance times of the fore‐ and the hind‐limbs (i.e., forelimb stance time divided by hindlimb stance time) was determined. Treadmill speed had to be matched more or less to the preferred speed of the dogs (i.e., the speed at which they trotted most comfortably) in order to record as many valid strides as possible. Because absolute speed cannot be compared among different‐sized individuals, Froude number was calculated using equation (4): Froude number ¼ v2=g l

ð4Þ

Here, v represents absolute speed (in m/sec), g is gravitational acceleration (9.81 m/s2) and l is hindlimb length (based on Alexander and Jayes, '83). Average forelimb angle during stance was determined as the average of the angle between the vertical and the line connecting the scapular and foot markers at touchdown and the angle between the vertical and the line connecting these markers at liftoff (Fig. 2). Similarly, average hindlimb stance angle was calculated as the mean of the angle between the vertical and the lines connecting the hip joint with the foot marker at touchdown and liftoff, respectively. Limb protraction is indicated by positive values, retraction by negative ones. Note that averaging touchdown and liftoff positions assumes the limb to move at constant angular velocity during stance and thus this average value to represent mid‐stance position. Because limbs typically move faster prior mid‐stance than after, the error generated by this method biases the limbs' positions towards protraction. Therefore, the method used potentially underestimated the increasing limb retraction observed herein (see Results Section). To evaluate changes in trunk shape, the diameters of the thorax and the abdomen were measured in the photographs using Adobe Photoshop (Version 5). The thoracic diameter was determined posterior to the forelimb at the deepest point of the sternum; the abdominal diameter was measured cranial to the prepuce (Fig. 1). Then, the ratio of the two lengths was calculated. A ratio of 1.0 indicates a rectangular area in the image (i.e., a cylindrical trunk shape), while a ratio >1.0 indicates a trapezoid (i.e., a conical trunk shape with the abdominal diameter being smaller than the thoracic one). Statistics The data were tested for normal distribution using the Kolmogorov–Smirnov test. Differences in vertical force, stance duration and thorax‐to‐abdomen ratios as well as average forelimb angles and age were tested among groups using a one‐ way analysis of variance (ANOVA) for repeated measures followed by post hoc Tukey's test. Differences between average hindlimb angles and age were tested using a one‐way ANOVA followed by post hoc Tukey's test because of the missing data from three dogs. P‐values of P < 0.05 were considered significant. Statistical analyses were done using GraphPad Prism (Version 4, GraphPad Software, Inc., California Corporation, CA, USA). J. Exp. Zool.

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Table 1. Symmetry indices (mean  SD in %) of the vertical force parameters for all dogs at the different ages. Peak vertical force

Vertical impulse

PW

Forelimb

Hindlimb

Forelimb

Hindlimb

11 13 19a 22 26 30 43 51

0.2  1.5 0.9  1.7 0.2  0.4 0.3  1.3 0.4  1.6 0.2  0.9 0.1  1.8 0.3  2.7

0.2  1.3 1.7  2.5 0.0  1.3 0.3  1.7 0.1  1.6 0.4  2.0 1.0  1.9 0.5  1.6

0.2  4.1 0.8  4.3 1.9  1.4 0.1  4.4 0.3  3.3 0.7  3.9 0.3  3.6 0.2  1.9

4.4  4.5 0.9  3.6 0.2  3.7 1.6  5.7 2.5  5.6 1.5  4.3 1.2  3.3 1.0  7.1

Perfect symmetry is given at SI ¼ 0. Physiological ranges are up to 4% and 6% difference for the fore‐ and the hind‐limbs, respectively (Budsberg et al., '93). Negative values indicate that the parameters were greater for the right than the left limb; positive values indicate the reverse. PW, postnatal week; SD, standard deviation. a Note that two individuals were measured at PW20.

RESULTS At all ages, the symmetry indices were within the normal ranges observed for adult dogs. Hence, the puppies were sound during the data collection and the data from the two body sides were pooled (Table 1). Furthermore, the puppies' force parameters were as symmetrical as those of adult dogs despite the puppies' seemingly more irregular gait. During the course of the study, the dogs' preferred trotting speeds increased and therefore the Froude number differed slightly but significantly between the first and the last recordings (PW11: 0.5  0.1 (mean  standard deviation), PW51: 0.9  0.1; Table 2).

Consequently, younger dogs trotted at treadmill speeds at which they still walked when older. Because vertical force parameters depend on speed (see Discussion Section), we will focus on fore‐ to hind‐limb ratios of these parameters in the following Table 3. At all ages, peak force and impulse were significantly greater in the forelimbs than the hindlimbs, indicating a greater role of the forelimbs in weight support at all ages (Fig. 3; Table 4). The ANOVA revealed that both peak force and impulse showed significant differences among the ages; with age, they increased in the forelimb and consequently decreased in the hindlimb. Accordingly, the fraction of the BW supported by the forelimbs increased from 59.2  1.7% to 62.9  1.9% (peak force) while that of the hindlimbs decreased from 40.8  1.7% to 37.1  1.9% during the course of the study (Table 5). Similarly, vertical impulse shifted by ca. 4% of the BW from caudal to cranial (forelimbs: 62.4  4.7% to 66.5  0.7%; hindlimbs: 37.6  4.7% to 33.6  0.7%). The ratio between fore‐ and hind‐limb stance times increased significantly; thus, stance time of the forelimb increased relative to the stance time of the hindlimb (Table 2). While the time to peak vertical force did not change with age in the forelimbs, it increased significantly in the hindlimb indicating that maximum force occurred earlier during stance when the dogs were younger (Table 6). With age, fore‐ and hind‐limb angles at touchdown decreased significantly, while limb angles at liftoff were unchanged (Table 7). In result, both average fore‐ and hind‐limb angles increased during ontogeny (i.e., limbs were increasingly retracted during stance). At all ages, the forelimbs were overall more protracted than the hindlimbs as the consistently greater touchdown and liftoff angles as well as the greater average limb angles indicate (Table 7). The ratio of the thoracic versus the abdominal diameter indicates that the trunk shape of the puppies was nearly cylindrical (i.e., thorax‐to‐abdomen ratio 1.1 at PW11; Table 6). During the study period, the thorax‐to‐abdomen ratio increased significantly,

Table 2. Stance duration (mean  SD in seconds) for the fore‐ and the hind‐limbs and stance duration ratio as well as Froude number (mean  SD) for all dogs at the different ages. PW

Forelimb

Hindlimb

Fore/hindlimb ratio

Froude number

11 13 19a 22 26 30 43 51

0.20  0.01 0.22  0.01 0.23  0.01 0.23  0.01 0.22  0.00 0.22  0.01 0.22  0.00 0.21  0.01

0.19  0.01 0.20  0.01 0.22  0.01 0.21  0.01 0.19  0.01 0.19  0.01 0.18  0.01 0.18  0.02

1.05  0.06a 1.07  0.02b 1.06  0.02c 1.09  0.05d 1.15  0.05a,b,c 1.16  0.05a,b,c 1.18  0.05a,b,c,d 1.15  0.08a,b,c

0.53  0.09a 0.52  0.09b 0.56  0.04c 0.62  0.04d 0.78  0.05a,b,c,d,e 0.85  0.06a,b,c,d 0.87  0.08a,b,c,d 0.93  0.11a,b,c,d,e

PW, postnatal week; SD, standard deviation. Paired letters in subscript refer to a significant difference (P < 0.05) between the respective ages using Tukey's post hoc test. For example, Froude number at PW11 is significantly different from the values from PW26 on. a Note that two individuals were measured at PW20.

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Table 3. Vertical force parameters (mean  SD in %BW and %BWs, respectively) for all dogs at the different ages. Peak vertical force

Vertical impulse

PW

Forelimb

Hindlimb

Forelimb

Hindlimb

11 13 19a 22 26 30 43 51

101.0  7.0 107.1  6.4 114.1  3.1 118.0  6.4 124.1  5.8 127.4  4.7 125.9  3.4 124.4  5.3

69.9  7.1 69.7  4.3 70.7  5.7 73.2  4.6 73.7  5.7 75.0  9.0 71.9  5.6 73.3  4.8

12.1  1.8 12.8  0.8 13.9  0.8 14.4  0.7 14.1  0.5 14.1  0.4 14.2  0.7 13.5  0.5

7.2  0.5 7.5  0.7 8.3  0.5 8.3  0.5 7.3  0.4 7.3  0.5 6.9  0.3 6.8  0.3

PW, postnatal week; SD, standard deviation. a Note that two individuals were measured at PW20.

so that the trunk shape resembled a frustum at the end of the study (i.e., thorax‐to‐abdomen ratio 1.3 at PW51; Table 6).

DISCUSSION Influence of Speed on Force and Stance Parameters In the current study, Froude number significantly increased between 11 and 51 weeks of postnatal age. Because many gait parameters depend on locomotor speed, the observed changes in the vertical force and the stance time ratios may potentially result from differences in speed rather than age. In adult dogs, for example, peak vertical force increases and vertical impulse decreases with increasing trotting speed (Riggs et al., '93; McLaughlin and Roush, '94; Voss et al., 2010). Because maximum force increases more in the forelimbs than the hindlimbs when dogs trot faster, the increase in the fore‐ to the hind‐limb peak ratio observed in the current study may partially be explained by the increase in relative speed with age. However, compared with the change in the peak vertical force ratio observed in this study (ca. 4%), the speed‐related changes reported for adult dogs across a similar change of relative speed were small (ca. 2%; Riggs et al., '93; McLaughlin and Roush, '94). Furthermore, in adult trotting dogs, the vertical impulse of fore‐ and hind‐limbs decreases at similar rates with increasing speed and therefore impulse ratio is independent of speed (Riggs et al., '93; McLaughlin and Roush, '94; see also Witte et al., 2004). In contrast, the fore‐ to the hind‐limb impulse ratio increased significantly with age in the current study; that is, the forelimbs' vertical impulse was relatively larger when the dogs were older. This observation resembles results from adult dogs, in which experimental loading of the pectoral girdle resulted in an increase of the vertical impulse ratio (Lee et al., 2004). In summary, our data suggest that the forelimbs support a relatively smaller proportion of the BW in puppies than adult dogs.

Similar to other mammals, when dogs increase locomotor speed, stance time decreases (e.g., Arshavskii et al., '65; McLaughlin and Roush, '94; Maes et al., 2008). Because stance duration decreases more in the forelimbs than the hindlimbs, stance time ratio decreases when adult dogs trot faster (McLaughlin and Roush, '94). In contrast, the stance time ratio between fore‐ and hind‐limbs increased during the course of this study despite an increase in relative speed. Relative fore‐ and hind‐limb duty factors have been suggested to reflect the antero‐posterior mass distribution of trotting quadrupeds and adding mass to the forelimb led to an increase in the fore‐ to hind‐limb stance time ratio (Lee et al., 2004). Therefore, the increase in the stance time ratio observed herein corroborates our conclusion of the increasing support role of the forelimbs when dogs grow. Ontogenetic Changes in the Support Patterns in Dogs Many studies have shown that dogs bear a greater proportion of their BW on the forelimbs (e.g., Krüger, '43; Bryant et al., '87; Budsberg et al., '87; Rumph et al., '94; DeCamp, '97; Lee et al., '99; Bertram et al., 2000; McLaughlin, 2001; Fanchon et al., 2006; Bockstahler et al., 2007; Walter and Carrier, 2007; Katic et al., 2009; Mölsa et al., 2010; Kim et al., 2011; Voss et al., 2011) and this is, as this and one previous study examining dogs between PW4 and PW15 show (Biknevicius et al., '97), true from early on in life. Therefore, in puppies and adult dogs, the forelimbs consistently play a greater role in supporting the body than the hindlimbs. At the end of this study, at PW51, load distribution of our dogs was comparable with other adult individuals of the same breed (Abdelhadi et al., 2013; Fischer et al., 2013). How much of the BW the fore‐ versus the hind‐limbs support in adult dogs, however, differs among breeds. Sighthounds such as Greyhounds or Borzoi show lower vertical force ratios compared to other breeds such as Labrador Retriever, Rhodesian Ridgeback, or Rottweiler (Krüger, '43; Bertram et al., 2000; Mölsa et al., 2010; J. Exp. Zool.

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Figure 3. Vertical force curves of the fore‐ and the hind‐limbs time‐normalized to the stance duration of the forelimbs. Plotted are the means from the six dogs, error bars indicate standard deviation. Note, the decrease of the hindlimb's stance time relative to that of the forelimbs and the increasing force difference between fore‐ and hind‐limbs.  Two dogs had to be studied at PW20. PW, postnatal week.

Kim et al., 2011; Voss et al., 2011). Thus, depending on morphology (i.e., the anterior–posterior body mass distribution) and maybe less on limb posture (Fischer and Lilje, 2011), the fore‐to‐hind weight support varies among breeds. J. Exp. Zool.

Similarly, morphological variation due to growth results in changes in the weight‐supporting characteristics of fore‐ versus hind‐limbs in developing mammals (Grand, '77; Kimura, '87, 2000; 2000; Turnquist and Wells, '94; Grand and Barboza, 2001; Shapiro

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Table 4. Mean ratios (mean  SD) of load distribution between the fore‐ and the hind‐limbs and support factor for the forelimbs of all dogs at the different ages. PW

Peak vertical force

Vertical impulse

Support factor

11 13 19a 22 26 30 43 51

1.45  0.10a 1.54  0.12b 1.62  0.16 1.62  0.13 1.69  0.17a 1.72  0.22a 1.76  0.16a,b 1.70  0.15a

1.70  0.38a 1.70  0.08b 1.67  0.09c 1.73  0.09d 1.93  0.12 1.95  0.13 2.07  0.08a,b,c,d 1.98  0.06c

0.62  0.05a 0.63  0.01b 0.63  0.01c 0.63  0.01d 0.66  0.01 0.66  0.02 0.67  0.01a,b,c,d 0.66  0.01a,c

PW, postnatal week; SD, standard deviation. For explanation of the subscripts, see Table 2. a Note that two individuals were measured at PW20.

Table 5. Mean load distribution (mean  SD in %) between the fore‐ and the hind‐limbs of all dogs at the different ages. Vertical impulse

PW

Forelimb

Hindlimb

Forelimb

Hindlimb

11 13 19a 22 26 30 43 51

59.2  1.7a 60.6  1.8b 61.8  2.2 61.7  1.9 62.8  2.4a 63.1  2.9a,b 63.7  2.1a,b 62.9  1.9a

40.8  1.7a 39.4  1.8b 38.2  2.2 38.3  1.9 37.2  2.4a 36.9  2.9a 36.3  2.1a,b 37.1  1.9a

62.4  4.7a 63.0  1.0b 62.5  1.2c 63.3  1.2d 65.8  1.4 66.0  1.6 67.4  0.8a,b,c,d 66.5  0.7a,c

37.6  4.7a 37.0  1.0b 37.5  1.2c 36.7  1.2d 34.2  1.4 34.0  1.6 32.6  0.8a,b,c,d 33.6  0.7a,c

PW, postnatal week; SD, standard deviation. For explanation of the subscripts, see Table 2. a Note that two individuals were measured at PW20.

PW

Forelimb

Hindlimb

Thorax/abdomen ratio

Body mass

11 13 19a 22 26 30 43 51

47.7  4.1 44.8  4.8 42.4  2.2 44.5  2.4 45.3  2.2 45.5  2.1 44.7  1.7 46.4  1.3

39.8  3.3a 41.8  2.6b 44.6  2.9a 45.6  2.5a 46.7  2.8a,b 45.3  1.1a 46.5  2.1a,b 46.2  0.9a,b

1.09  0.06a 1.07  0.04b 1.13  0.05c 1.21  0.05a,b,d 1.21  0.06a,b,e 1.28  0.06a,b,c 1.31  0.05a,b,c,d,e 1.27  0.05a,b,c

6.64  0.63 7.73  0.60 12.73  1.32 13.48  1.32 14.73  1.51 15.49  1.99 17.00  1.99 18.42  1.86

PW, postnatal week; SD, standard deviation. For explanation of the subscripts, see Table 2. a Note that two individuals were measured at PW20.

and Raichlen, 2006; Young, 2012). Both vertical force and stance time ratios evaluated in the current study indicate a cranial shift in the support roles in growing dogs. This is in contrast to the previous ontogenetic studies, which consistently show a caudal shift in the support pattern (i.e., decreasing forelimb and conversely increasing hindlimb support; Grand, '77; Kimura, '87; 2000; Turnquist and Wells, '94; Grand and Barboza, 2001; Shapiro and Raichlen, 2006; Young, 2012). At least three observations are consistent with the cranial shift in the support roles in growing dogs. First, the postural index (i.e., withers or pelvic height divided by the sum of the segment lengths) increases more in the hindlimbs than the forelimbs (from 0.86 to 0.94 and 0.76 to 0.80 between PW11 and PW51, respectively; D. Helmsmüller, unpublished data). Therefore, similar to growing

Peak vertical force

Table 6. Time to peak force (mean  SD in % of stance duration) of the fore‐ and the hind‐limbs, thorax‐to‐abdomen ratio (mean  SD), and mean body mass (mean  SD) for all dogs at the different ages.

horses (Grossi and Canals, 2010), older dogs have relatively more erect hindlimbs than when they are younger. The increasingly erect hindlimbs result in a postural change of the body that is consistent with a greater support role of the forelimbs. Second, average limb angles decreased in both fore‐ and hind‐ limbs during the study period due to a decreasing protraction of the limbs at touchdown. In result, the older the dogs, the more retracted were their limbs. All other factors being equal, more retracted fore‐ and hind‐limbs increase the percentage of BW borne by the forelimbs (Raichlen et al., 2009). Therefore, the cranial shift in support roles is likely brought about by the ontogenetic changes in average limb position. In addition, the average forelimb angle decreased more than the average hindlimb angle; that is, the forelimbs became relatively more retracted during development than the hindlimbs. Because increased forelimb retraction places the forefeet closer to the CoM and thereby increasing forelimb support (Gray, '44), the dogs also supported relatively more weight on their forelimbs when they were older due to their more retracted forelimbs. The third argument consistent with a cranial shift in support roles is that puppies have a relatively voluminous belly and a cylindrical trunk compared to the conical trunk form that adult dogs show. Abdominal organs such as spleen or kidneys show negative allometry, while the heart (Lützen et al., '76; but see Deavers et al., '72) and the stomach exhibit positive allometry in various mammals (guinea pig: Bessesen and Carlson, '23; dog: Deavers et al., '72; Lützen et al., '76; rat: Stewart and German, '99). Furthermore, to fuel ontogenetic growth and provide the developing body with the tissue necessary for digestion and absorption of high dietary loads, the small intestine is relatively larger in juveniles. For example, Beagle puppies at PW9 have, J. Exp. Zool.

262

HELMSMÜLLER ET AL.

Table 7. Fore‐ and hind‐limb angles at touchdown and liftoff (top) as well as average limb angle during stance (mean  SD in). Forelimb PW 11 13 19a 22 26 30 43 51

Hindlimb

Touchdown

Liftoff

Touchdown

Liftoff

23.4  1.9a 22.4  3.8b 20.1  4.1 20.1  2.2c 16.1  4.0a,b 17.2  2.5a,b 15.3  4.2a,b,c 15.3  3.6a,b,c

25.1  3.6 26.8  5.5 27.6  4.4 28.3  3.5 30.0  3.5 28.7  2.0 29.6  2.9 28.6  3.0

17.0  1.9a 16.3  2.1b 14.9  2.3 13.6  2.6 10.0  3.1a,b 10.7  2.4a 10.8  3.7a 10.7  2.7a,b

34.7  2.0 44.1  1.6 31.3  1.2 32.5  1.5 31.5  2.1 31.5  2.1 31.0  3.0 31.7  2.9

11 13 19a 22 26 30 43 51

Average forelimb angle

Average hindlimb angle

0.9  2.2a 2.2  4.5 3.8  4.0 3.9  2.6 6.9  5.6a 5.8  1.5 7.2  3.3a 6.7  3.1a

8.8  0.4a 5.9  4.7 8.2  0.9b 7.9  4.0 10.7  1.1a,b 10.4  0.7b 10.1  1.2b 10.5  1.1b

Positive values indicate that the limb is protracted; negative values indicate that the limb is retracted. The limbs are increasingly retracted with age due to decreasing touchdown angles. Note that the hindlimbs of two ( ) or one ( ) individual could not be analyzed for this age. SD, standard deviation; PW, weeks postnatal. For illustration of the angle definitions, see Figure 2. For explanation of the subscripts, see Table 2. a Note that two individuals were measured at PW20.

relative to body mass, a small intestine that is 33% longer, weighs 45% more, has 40% more mucosa and 35% more surface area than adults (Paulsen et al., 2003). Taken together, the growth patterns of the inner organs and particularly of the small intestine are in accordance with a cranial shift of the limbs' support roles. Although muscularity increases more in the hindlimbs than the forelimbs in cursorial mammals (e.g., bovids; Grand, '91), and dogs, as other mammals, show negative allometry of their heads (Helmsmüller et al., 2013), our results indicate that the growth patterns of the inner organs and the kinematic changes in limb position dominate the ontogenetic changes in the support pattern in dogs.

pattern. Needless to say, more data, particularly from other forelimb‐dominated species, are necessary to test this hypothesis. Of the characteristics suggested to explain differences in the support patterns—morphology, limb position, muscle activity—we were able to evaluate only two but both show developmental changes consistent with a cranial shift in weight support.

ACKNOWLEDGMENTS We thank J. Abdelhadi, S. Fischer, V. Galindo‐Zamora, and P. Wefstaedt for discussions, K. Lucas for technical assistance and the animal keepers of the Small Animal Clinic for their support. Comments provided by Jesse W. Young and a second reviewer greatly improved the manuscript and were very much appreciated.

CONCLUDING REMARKS Contrary to previous studies on hindlimb‐dominated species (i.e., mainly primates), this investigation in dogs shows that not all mammals display a caudal shift in their limbs' support roles during ontogeny. Rather, growing dogs carry an increasing proportion of BW on their forelimbs. Albeit based on a small sample, we propose forelimb‐dominated species (i.e., most non‐primates), if at all, to augment the role that their forelimbs play in weight support, while hindlimb‐dominated species display the opposite ontogenetic J. Exp. Zool.

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Ontogenetic change of the weight support pattern in growing dogs.

Weight support patterns vary widely among mammals. Differences in how much of the body weight is supported by the fore- versus the hind-limbs are well...
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