erratum the movements of limb segments and joints...

$: Erratum The movements of limb segments and joints …jeb.biologists.org/content/jexbio/211/17/2735.full.pdf · ranges of motion during rapid locomotion, with this fraction increasing$
The movements of limb segments and joints during locomotion in African and Asianelephants

L. Ren, M. Butler, C. Miller, H. Paxton, D. Schwerda, M. S. Fischer and J. R. Hutchinson

10.1242/jeb.024364

There was an error published in J. Exp. Biol. 211, 2735-2751.

On p. 2740, in the section entitled ‘Limb motion during normal walking’, a character was missing in the second sentence such that thedegree of incline of the forearm, forefoot and thigh segments at mid-stance was incorrectly given as 411deg. rather than 4–11deg.

The text should have read:

‘At mid-stance, the forearm, forefoot and thigh segments were all relatively vertical (within 4–11deg.), whereas the upper arm, shank andhindfoot segments were less vertically inclined (–19, –23 and 38deg. to vertical, respectively).’

We apologise to authors and readers for this error.

Erratum

2735

INTRODUCTIONThe elephant hath joints, but none for courtesy. His legs are legs

for necessity, not for flexure.Ulysses in Act II, Scene iii (Shakespeare, 1609)

Elephants run straight-legged, thigh lined up with shank andupper arm with lower arm, so their legs look rather like mobile

Doric columns.p. 214 in (Bakker, 1986)

As the above quotes exemplify, humans have long recognizedthe distinctive columnar (straight-legged) limb posture of elephants.This recognition has generated classical misconceptions, such aselephants having no joints, no knees or four knees [e.g. pp. 101-109 in (Tennent, 1999)]. Ridiculous as those fallacies may seem tocontemporary scientists, elephant posture and gait remainmisunderstood, partly because of their strange anatomy and partlybecause of little rigorous measurement of elephant locomotion.Hence, potentially misleading oversimplifications persist, even inrecent comparative/functional studies (e.g. Bakker, 1986; Paul, 1998;Paul and Christiansen, 2000), and have become integrated intotextbook and popular media accounts. Elephants are unusual amongterrestrial animals not only in their enormous size [up to 7000kgin adult African elephants (Christiansen, 2004; Wood, 1972)] andapomorphically long limbs (Alexander et al., 1979a) but also in their

limited speed range [~7ms–1 maximum (Hutchinson et al., 2003)],continuous changes of kinematic patterns with increasing speed(Hutchinson et al., 2006) and smooth, relatively low-speed transitionto bouncing or ‘running’ hindlimb mechanics (Ren and Hutchinson,2008).

Earlier studies (Gambaryan, 1974; Hildebrand and Hurley, 1985;Marey and Pagès, 1887) provided basic descriptions of elephantsegment and joint motions that are widely cited and useful;however, these were largely qualitative, were based on smallsample sizes, and utilized ambiguous or technically limitedmethodology [e.g. 24 Hz video in (Hildebrand and Hurley, 1985);unknown elephant speeds in most studies]. Our initial studies(Hutchinson et al., 2003) showed that elephants shift from vaultingto bouncing hip motion, from slow to fast speeds; our later studies(Hutchinson et al., 2006) observed that hindlimb flexion seemedto increase concurrently, suggesting a shift from vaulting tobouncing limb mechanics (Ren and Hutchinson, 2008) aspreviously predicted. This limb flexion has not yet beenquantitatively measured or related directly to speed changes butdoes indicate marked differences in joint motion at least betweenthe forelimbs and hindlimbs. The differences between fore- andhind-foot posture and dynamics in elephants also relate to alteredloading and scaling of the bones and tendons (Miller et al., 2008).

The Journal of Experimental Biology 211, 2735-2751Published by The Company of Biologists 2008doi:10.1242/jeb.018820

The movements of limb segments and joints during locomotion in African and Asianelephants

Lei Ren1, Melanie Butler1, Charlotte Miller1, Heather Paxton1, Delf Schwerda2, Martin S. Fischer2 andJohn R. Hutchinson1,*

1Structure and Motion Laboratory, Department of Veterinary Basic Sciences, The Royal Veterinary College, University of London,Hatfield, Hertfordshire AL9 7TA, UK and 2Institut fuer Spezielle Zoologie und Evolutionsbiologie, mit Phyletischem Museum,

Jena 07743, Germany *Author for correspondence (e-mail: [email protected])

Accepted 15 May 2008

SUMMARYAs the largest extant terrestrial animals, elephants do not trot or gallop but can move smoothly to faster speeds without markedlychanging their kinematics, yet with a shift from vaulting to bouncing kinetics. To understand this unusual mechanism, wequantified the forelimb and hindlimb motions of eight Asian elephants (Elephas maximus) and seven African elephants(Loxodonta africana). We used 240Hz motion analysis (tracking 10 joint markers) to measure the flexion/extension angles andangular velocities of the limb segments and joints for 288strides across an eightfold range of speeds (0.6–4.9ms–1) and asevenfold range of body mass (521–3684kg). We show that the columnar limb orientation that elephants supposedly exemplify isan oversimplification – few segments or joints are extremely vertical during weight support (especially at faster speeds), and jointflexion during the swing phase is considerable. The ʻinflexibleʼ ankle is shown to have potentially spring-like motion, unlike thehighly flexible wrist, which ironically is more static during support. Elephants use approximately 31–77% of their maximal jointranges of motion during rapid locomotion, with this fraction increasing distally in the limbs, a trend observed in some otherrunning animals. All angular velocities decrease with increasing size, whereas smaller elephant limbs are not markedly moreflexed than adults. We find no major quantitative differences between African and Asian elephant locomotion but show thatelephant limb motions are more similar to those of smaller animals, including humans and horses, than commonly recognized.Such similarities have been obscured by the reliance on the term ʻcolumnarʼ to differentiate elephant limb posture from that ofother animals. Our database will be helpful for identifying elephants with unusual limb movements, facilitating early recognitionof musculoskeletal pathology.

Supplementary material available online at http://jeb.biologists.org/cgi/content/full/211/17/2735/DC1

Key words: elephant, proboscidea, joint, locomotion, biomechanics, speed, gait, kinematics.

THE JOURNAL OF EXPERIMENTAL BIOLOGY

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Our previous analysis of stride parameters (Hutchinson et al.,2006) demonstrated that elephants change speed by increasing stridefrequency, more than stride length, up to a dimensionless speed[û=v/(hg), where û is dimensionless speed, v is velocity, h is hipheight, and g is acceleration due to gravity] of 1.0. Beyond thisspeed, stride frequency approaches its maximum and stride lengthcontributes relatively more to speed increase. Correspondingly,stance time decreases most steeply with speed (continuing beyondû~1.5), with swing time reaching its plateau at û~1.0; concurrently,duty factor decreases sharply and then levels off. From theperspective of motion within the limbs, it is thus expected that, aselephants increase speed, they mainly increase joint/segment angularvelocities (required for larger stride frequencies) until runningquickly (û>1.0) when they rely more on greater joint rotations (largerranges of motion, perhaps including greater limb flexion) to generatethe longer strides observed.

In the present study, we analyze the coordination patterns of thelimb segments and joint movements during steady-state locomotionin Asian (Elephas maximus Linnaeus 1758) and African (Loxodontaafricana Blumenbach 1797) elephants. As noted above, elephantlimbs are the archetype for columnar, graviportal animals [large,relatively slow, with long proximal and short distal limb segments(Gregory, 1912)] and hence are of comparative interest, particularlyfor deciphering the relationships between body size and locomotorform and function. Therefore, our major aim is to determine howelephant limb motions compare with those of other mammalianspecies – are elephants always relatively restricted in theirjoint/segment ranges of motion, having less mobile joints than otheranimals? Are their limb motions fundamentally distinct from allother animals’, especially cursorially specialized forms, as they oftenhave been characterised (e.g. Bakker, 1986; Gregory, 1912; Paul,1998; Paul and Christiansen, 2000)? We sought to carefully examinehow useful and accurate the term ‘columnar’ is when applied toelephants.

Thus, we pose two fundamental questions here, related to theaims above. Firstly, what are the limb segment and joint angularand angular velocity changes across a normal walking stride inelephants, and how do motions differ within and between limbs?Particularly, just how columnar are elephants (i.e. what are theirsegmental and joint angles during locomotion)? Secondly, how doelephant limb motions change with speed, from slow walking to

fast running; i.e. does their ‘columnarity’ change with speed (aretheir legs always legs for necessity, not for flexure)? At all speeds,are all joints similarly columnar and of low flexibility/mobility oris there intra-/inter-limb diversity in joint flexibility (Gambaryan,1974; Hildebrand, 1984; Hildebrand and Hurley, 1985)? We testthe null hypothesis that joints all use a similar fraction of theirmaximal range of motion (i.e. that is allowed by joint surfaces andligaments) by comparing maximal in vivo (fast locomotion) vs invitro (cadaver manipulation) joint range of motion and discussalternative hypotheses.

We used motion analysis with 15 elephants covering a sevenfoldbody mass range to quantitatively answer these questions. Accuratebaseline joint and segment kinematic data are vital for furtherbiomechanical analyses, e.g. ‘internal work’ [movements ofsegments relative to the body’s center of mass (Hildebrand andHurley, 1985)], joint powers (e.g. Dutto et al., 2006), or inversedynamics analysis of muscle/bone stresses (e.g. Alexander et al.,1979b; Biewener, 1989; Biewener, 1990) of locomotion. Weexpected that there would be no major size/species differences inelephant kinematics (as in Hutchinson et al., 2006; Ren andHutchinson, 2008) but here search for any previously overlookeddifferences within limbs, as earlier studies have focused on whole-body or whole-limb kinematics. Another subsidiary goal of ouranalysis was to quantify how ‘normal’ elephant limbs move in orderto establish a comparative dataset for identifying foot, joint or otherlimb pathologies, which are a major concern for elephant keepers(Csuti et al., 2001; Egger et al., 2008).

MATERIALS AND METHODSAnimals

Table1 lists the animals we worked with and the zoos/parks wherethey were held. For Asian elephants, we used two juveniles(�5years old; 521 and 688kg body mass), two sub-adults (1740and 2072kg) and four adults (�20years old; 3149–3684kg bodymass). For African elephants, we used one juvenile (930kg), threesub-adults (2550–3230kg) and three adults (3100–3512kg). Ageswere known to trainers ±1year (or better for juveniles), and bodymasses were obtained using truck scales (±5kg) or a custom-madeforce platform apparatus (for Thailand elephants; constructed byArsalis Inc., Louvain-la-Neuve, Belgium; 7000kg max. load, 161m�1m plates). However, for the three adult African elephants

L. Ren and others

Table 1. Vital data for elephants used in this study

Age Mass Hip Shoulder No. of No. of Min. speed, Max. speed,Subject elephant Facility Species Sex (years) (kg) height (m) height (m) valid trials strides ms–1 (û) ms–1 (û)

A THUR African F 5 930 1.18 1.74 10 10 1.22 (0.36) 2.89 (0.86)B COLCH African F 26 3512 1.91 2.72 11 19 1.18 (0.27) 2.10 (0.48)C COLCH African F 23 3438 2.03 2.70 6 13 1.44 (0.33) 1.70 (0.39)D COLCH African F 23 3100 1.99 2.39 10 22 1.64 (0.37) 2.35 (0.54)E WMSP African M 13 3230 2.03 2.59 2 2 1.48 (0.34) 1.50 (0.35)F WMSP African F 14 2780 2.06 2.47 8 8 1.35 (0.31) 1.64 (0.37)G WMSP African F 13 2550 1.84 2.41 13 9 1.38 (0.32) 2.87 (0.67)H WHIPS Asian F 23 3684 1.70 2.00 10 36 0.95 (0.23) 3.73 (0.91)I WHIPS Asian F 23 3318 1.67 2.01 8 14 0.77 (0.19) 2.87 (0.71)J WHIPS Asian F 23 3161 1.56 2.03 9 16 0.85 (0.22) 3.37 (0.86)K WHIPS Asian F 23 3149 1.60 2.12 9 21 0.75 (0.19) 2.64 (0.66)L WHIPS Asian F 2 688 1.03 1.17 21 35 1.14 (0.36) 3.16 (1.00)M WHIPS Asian F 1.5 521 1.00 1.15 14 22 0.91 (0.30) 3.69 (1.20)N TECC Asian F 8 2072 1.51 1.92 18 33 1.03 (0.27) 4.45 (1.17)O TECC Asian M 6 1740 1.52 2.00 18 28 0.62 (0.16) 4.92 (1.29)

Facilities: THUR, Thüringer Zoo, Germany; COLCH, Colchester Zoo, UK; WMSP, West Midlands Safari Park, UK; WHIPS, Whipsnade Wild Animal Park, UK;TECC, Thailand Elephant Conservation Centre, Thailand.


2737Elephant limb motion

mass was unknown so it was estimated from publishedmass–shoulder height equations (Laws et al., 1975; Christiansen,2004). Hip and shoulder heights were measured from the groundto the approximate hip joint center or to the top of the scapula (Fig.1)respectively, with flexible measuring tape (±1cm) when the animalwas standing still. All studies were approved by The RoyalVeterinary College’s animal welfare and ethics board.

TrialsElephants were led by their handlers, using positive reinforcementsuch as food rewards and vocal commands, with the goal ofmaintaining a steady speed across a straight distance of ~15 m.They also had at least 5 m before and after this distance toaccelerate and decelerate to a steady speed, which, from previous

experience, we knew to be sufficient (Hutchinson et al., 2006).Trainers randomly varied the speed from slow walking to fastrunning across trials and allowed ample rest and food betweentrials to prevent fatigue. Experiments were cancelled if animalsshowed musculoskeletal pathology, fatigue or any other artifactsthat would cause discomfort or adversely affect our measurements.Handlers sought to build speed up to the near-maximal speed thatthe animal could achieve, which as usual among captive elephantswas below the top speeds observed in sleeker, more activeelephants [e.g. in Thailand 6.8 m s–1 (Hutchinson et al., 2003;Hutchinson et al., 2006)]. Data collection was conducted outdoors(during cloudy/twilight periods to reduce sunlight interferencewith our infrared motion capture) except at the Colchester Zoosite, when data were collected inside an elephant barn. All animals

Joint angles(2 segments)

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J

Fig. 1. Marker placements on arepresentative African elephant.(A) Subject G (Table 1) in oblique rightlateral view showing all skin markers (backmarkers shown are not used in this study).(B) Relationship of markers with underlyingskeleton. (C) Definitions of segment andjoint angles [picture modified fromShoshani (Shoshani, 1992)]. Palpatedanatomical positions of markers (Smutsand Bezuidenhout, 1993; Smuts andBezuidenhout, 1994): lateral side ofgreater tubercle of humerus, lateralepicondyle of humerus, styloid process ofulna, toenail of manus digit 3, caudal sideof accessory carpal, greater trochanter offemur (just caudal to tuber coxae of ilium),lateral epicondyle of femur (just caudaland proximal to patella), lateral malleolusof fibula, middle of toenail of pes digit 3,caudal side of calcaneal tuber. We onlyused the calcaneus and carpal markers toidentify touch-down/lift-off events (seeMaterials and Methods). The segmentalangles were calculated relative to a verticalline through the proximal marker of eachsegment; only shown precisely for theupper arm and thigh segments.


2738

were moving over very firm (concrete, asphalt, packed dirt orforce platform) and level substrates.

Marker placement and motion captureInfrared-reflective tape (Scotchlite 8850; 3M, Manchester, UK)covering styrofoam hemispheres (7cm diameter for all elephants,except the juveniles, for which 3.5cm diameters were used) wereattached to the skin with double-sided carpet tape, over palpablelandmarks. Fig.1 explains these landmarks and positions. The ears(particularly in African elephants) hid the shoulder marker in sometrials so data on the upper arm segment and elbow joint angle arescarcer. Due to time constraints (sunlight, animal and traineravailability, and manageability) the number of markers we coulduse was limited. This was exacerbated by the tendency of elephantsto intentionally or accidentally dislodge or destroy markers. Weconsidered using multiple-marker clusters to rigorously quantify 3Dlimb motions (e.g. Cappozo et al., 2005; Rubenson et al., 2007) butthis was judged to be impossible under the constrained conditions.

A synchronized six-camera Qualisys (Gothenburg, Sweden)MCU 500 system (240Hz) was used to record elephant limb markermotions, digitally triggered at the start of each trial. The system wascalibrated before and after trials to a 3-D measurement accuracy of~1mm. Total capture volume varied with ambient light and otherconditions but was generally ~12m�3m�4m. Animal forwardvelocity for each stride was measured by calculating the averagesof the hip and shoulder marker velocities. We defined steady-statetrials as those in which the absolute difference between the forwardvelocities at two consecutive heel strikes was less than 20% of theaverage forward velocity. Trials with greater or smaller values ofacceleration/deceleration were discarded. Froude numbers[Fr=v2/(hg)] and dimensionless speed (û=Fr0.5) were calculated tonormalize speeds (e.g. Alexander and Jayes, 1983) for comparisonbetween elephants of different sizes and with previous strideparameter data (Hutchinson et al., 2006).

To estimate maximal joint ranges of motion, we conducted invitro studies with fresh cadaveric limb material (joint capsulesand ligaments intact, skin and muscles removed) of one juvenileAsian elephant (830 kg body mass; 3 years old at death) that hadno significant musculoskeletal pathologies. We used the samemotion capture system described above but with the cameras ina ring around the specimen, and 2.5 cm diameter markers attachedon bony landmarks and anatomical reference points (total of atleast five markers per segment) to calculate the sagittal plane jointmotions (detailed below) of the hip, shoulder, knee and elbowjoints. We captured a static pose emulating standing posture (forcalibration of distances between markers), then manually flexedand extended each joint, one at a time, through its maximal rangeof motion for five trials per joint. Measurements on an additionaladult elephant cadaver were performed but we were unable tosafely apply sufficiently large loads to cover a plausibly largerange of motion. For comparisons with other species, weconducted the same in vitro measurements with the forelimbs andhindlimbs of one Dutch Warmblood horse (adult, previouslyhealthy, 500 kg body mass) using the same markers as Back etal. (Back et al., 1995a; Back et al., 1995b) and collated literaturedata for cats, dogs and humans (see Discussion).

Angle and angular velocity calculationsAll motion analysis 3-D coordinate data were first filtered using alow-pass, zero-lag Butterworth digital filter [fourth order, cut-offfrequency 8Hz (Winter et al., 1974)]. We calculated the sagittalplane (approximated as the plane parallel to the mean direction of

motion in each trial) motions of the upper arm, forearm, forefoot(manus), thigh, shank and hindfoot (pes) segments and the elbow,wrist, knee and ankle joints. Segmental angles were ‘external’ anglesmeasured with respect to the vertical. Joint angles were the ‘internal’angles between two articulated segments. As there were norepeatable landmarks on the scapula or pelvis that we trusted tohave minimal skin motion, we did not measure shoulder or hip jointangles, although our upper arm and thigh segmental angles areroughly comparable to these. More detailed analyses of 3-Dkinematics and skin motion for these two joints and the scapulasegment [a critical component of mammalian limb motion (Fischerand Blickhan, 2006; Fischer et al., 2002)] are still needed. Qualitativeestimates of segment abduction and adduction can be made usingour data (as the motion capture is inherently 3-D; see Discussionfor qualitative descriptions of these motions) but here we focusprimarily on sagittal plane motions as these are clearly the dominantcomponent of elephant limb motion. Angular velocities of jointsand segments were calculated using a first-order finite differentiationmethod (Pezzack et al., 1977).

We divided trials into their component strides by identifying thestance and swing phases for each limb. Limb touch-down wasdefined as when the vertical position (extracted from our motioncapture data) of the fore- or hindfoot carpal or tarsal marker reachedits minimum. Limb lift-off was defined as when the fore or hindlimb middle toe marker (Fig. 1) reached its lowest position(Hutchinson et al., 2006) (Fig.2). The resulting duty factors matchedthose at comparable speeds from video data (Hutchinson et al.,2006), validating this approach and avoiding a reliance on lower-resolution video footfall identification.

Although we depict angular motions and velocities for all studiedelephant segments and joints across whole strides, for statisticalcomparisons we chose reference events during the stride to compareamong elephants. For stance phase, we used touch-down, mid-stance(50% of stance time) and lift-off events as reference events. It ismore difficult to quantify reference events in the swing phase butwe selected minimal and maximal angle (or angular velocity) duringthe swing phase to emphasize the full range of motion used; in thepresent study we simply refer to these as minimal swing and maximalswing. Finally, the maximal value of each parameter minus theminimal value for the entire stride was the range of motion (ROM)for angles, and range of angular velocity (RAV) for angularvelocities. These two parameters capture the widest excursions orrotational speed variations of the joints and hence are ofbiomechanical and functional significance although, like minimaland maximal swing, they are not always necessarily anchored tothe same point in each stride.

As suggested by our marker placement repeatability assessment(see Results), we identified (post hoc) moderate offsets in someangle measures vs stride time (i.e. % gait cycle) that were probablycaused by inaccurate marker placements, although most of theangle measures were repeatable. In these cases, to minimize thebias these offsets would bring into our statistical analyses, thewhole angular displacement curves for a stride were shifted sothat the mid-stance angles matched the mean mid-stance anglefor all elephants. As the angular velocity is insensitive to thismarker placement offset, this error does not affect thosemeasurements. Similar relative offset errors are presumablypresent in most other studies of animal limb motion but are seldomdiscussed or investigated.

Our in vitro cadaveric studies calculated sagittal plane jointmotions more rigorously as they used multiple markers attacheddirectly to the skeleton. To quantify the total ROM of each joint

L. Ren and others



we simply used the 3-D coordinates of each joint marker to quantifythe sagittal plane joint angles in maximal flexion and extension.

Marker placement repeatability assessmentOne might expect that the positioning of skin-mounted motioncapture markers would be hard to reproduce on multiple animalsor experiments with the same animal. Therefore, we conducteda basic initial analysis of how consistently we were positioningthe skin markers. The same investigator (J.R.H.) placed all 10markers on two African elephant subjects (B and C in Table 1).The elephants did four trials of normal walking at the same speed,then the markers were removed and replaced with a new set. Thiswas repeated 10 times for subject B and five times for subject C.We calculated the mid-stance segment (for upper arm and thigh)or joint angles as above and analyzed the results statistically asbelow.

Soft tissue artifacts (caused by the skin/muscles moving withrespect to the underlying bones) are also certainly a problem forstudies of elephant joint motion, perhaps more so than in smalleranimals. Absolute error in estimating skeletal joint centers usingskin markers is large, and the mobile, thick skin of elephants mayalso cause large relative errors. Invasive bone pin measurements(Reinschmidt et al., 1997; van Weeren et al., 1988; van Weerenet al., 1990) are impossible, and elephants are too large forcineradiographic imaging studies of joint motion (e.g. Cappozzoet al., 1996; Filipe et al., 2006; Gatesy, 1999). However, studiesof human and horse skin marker accuracy show that errors incalculating flexion and extension angles are relatively minor,especially for distal joints (Back et al., 1995a; Back et al., 1995b;Leardini et al., 2005; Reinschmidt et al., 1997; van Weeren etal., 1988; van Weeren et al., 1990). Therefore, we assume thatour flexion/extension measurements are reasonably accurate,pending more exhaustive in vitro and in vivo analyses.

Statistical analysisAll statistical analyses were conducted using SPSS 15.0 software(SPSS, Inc., Chicago, IL, USA). The effects of locomotor speed,species and body mass on angles and angular velocities wereanalyzed using analysis of variance (ANOVA) with repeatedmeasurements via a linear mixed model approach by taking intoaccount of the intra- and inter-subject variability. The different speedranges, elephant species and body mass ranges were the fixed effects,and elephants were random effects. Differences between each pairwere tested using Fisher’s least significant difference (LSD) multiplecomparison based on the least-squared means. This approach waschosen to maximize the amount of usable data, as opposed toregression techniques.

Our marker replacement repeatability test involved anindependent simple t-test for each segment or joint at mid-stance(between elephant differences), a one-way ANOVA to test for theeffect of trial number, and a one-sample Kolmogorov–Smirnov testfor normal distribution of segment or joint angles between markersets. The effect of speed was removed via a Pearson’s two-tailed t-test for correlation between speed and mid-stance angle. A linearcurve fit equation was then used to remove speed effects if aspeed–angle correlation was present. For normally distributedangles we used a two-way ANOVA to test the influence of markerset on angle (non-normally distributed angles were omitted).Statistical significance was considered as P<0.05.

RESULTSIn total we collected 167 trials and 288 strides of data for our 15elephants, with a roughly eightfold mean forward velocity range of0.62–4.92ms–1. Our in vitro analysis provided 18 valid trials ofmaximal joint ROM for the juvenile elephant (only three valid trialsfor the wrist) and 20 valid trials for the horse (horse data arepresented in the Discussion). Where particular values for angles or

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Fig. 2. Representative limb segment angular trajectories during a stride for an elephant (Subject H, Table 1) moving at normal walking speed; 1.37±0.28 m s–1

(Fr=0.11; N=5). Stance phase is shown in blue; swing phase in red. Note that the stance phase for the forelimb (right side) is offset ~15% of a stride relativeto the hindlimb, as the data were collected synchronously; this relative limb phase offset is typical for a lateral sequence walk in elephants (Hutchinson etal., 2003; Hutchinson et al., 2006).


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angular velocities are shown below, mean values are used; the Tables(Tables 2–4; supplementary material Tables S1– S7) show thestandard errors and N values.

Marker placement repeatability assessmentSubjects B and C had mean (±s.d.) walking speeds of 1.08±0.17ms–1

and 1.52±0.36ms–1, respectively, ranging from 0.68 to 1.49 and0.59 to 2.15ms–1. As the ears hid some skin markers, mid-stanceupper arm and elbow joint measurements were only available forsubject B (N=18 and 12, respectively). For the wrist, thigh, kneeand ankle we obtained 88/52, 76/57, 63/57 and 66/49 valid stridesof data for the two subjects.

As the two subjects showed statistically significant differences(P<0.05), they were treated separately. No effect of trial numberwas found (P>0.05). The mid-stance angle data were all normallydistributed except for the thigh and wrist from subject B (whichwere not subsequently analyzed). Speed only had a significant effecton subject B’s knee joint angle and subject C’s thigh segment angle(P<0.01), as the speed range was narrow. Except for these lattertwo angles, which showed a significant difference between markersets (P<0.05), and the two excluded for non-normally distributeddata, the remaining six angles showed a repeatable pattern at mid-stance (P>0.05).

Post hoc examination of the significantly different or non-normally distributed angles (and outliers) showed that, in mostcases, markers had been replaced in positions that were slightlyoffset from the normal position, offsetting the entire segment/jointangle vs stride time curves upward or downward ~5–10 deg. (cf.Figs 2–4); if manually shifted back to lie over the mean values(see Materials and methods), these differences disappeared. Theseresults indicated that the placement of the skin markers wasrepeatable when conducted by the same experienced investigatorand also that we needed to correct for offset angle vs stride timecurves.

Limb motion during normal walkingAt a comfortable walking speed (Fr~0.10), elephant limb segmentand joint motions throughout the stride were generally quite smooth(Fig2 and Fig3). At mid-stance, the forearm, forefoot and thighsegments were all relatively vertical (within 4 11deg.), whereas theupper arm, shank and hindfoot segments were less verticallyinclined (–19, –23 and 38 deg. to vertical, respectively).Correspondingly, the elbow, wrist and knee joints were fairlyextended at mid-stance (157deg., 186deg. and 152deg.) but theankle joint was more flexed (117deg.). Touch-down and lift-offangles varied by <20deg. from these values.

L. Ren and others

Table 2. Limb segment and joint angle (deg.) data of all individuals of both species during walking (û = 0.25–0.50)

Stance Swing

Segment or joint Touch-down Mid-stance Lift-off Min. Max. Range of motion

ForelimbUpper arm –1±1 (14) –19±1 (14) –39±2 (14) –41±2 (8) 1±2 (8) 44±2 (8)Forearm 28±1 (26) 5±1 (25) –8±1 (25) –8±2 (19) 38±1 (19) 52±1 (18)Forefoot 27±1 (20) 11±1 (20) –28±2 (20) –48±1 (14) 36±1 (14) 90±2 (14)Elbow joint 150±2 (14) 157±1 (14) 146±2 (14) 122±1 (8) 148±2 (8) 36±1 (8)Wrist joint 177±1 (20) 186±1 (20) 162±2 (20) 123±1 (14) 178±1 (14) 66±1 (14)

HindlimbThigh 21±1 (22) 4±1 (25) –2±1 (26) –2±1 (25) 24±1 (25) 29±1 (21)Shank 2±1 (25) –23±1 (26) –47±1 (26) –50±1 (25) 7±1 (25) 55±1 (24)Hindfoot 51±1 (25) 38±1 (25) –5±1 (25) –20±1 (19) 56±1 (19) 76±1 (19)Knee joint 160±1 (22) 152±1 (25) 134±1 (26) 122±1 (25) 163±1 (25) 42±1 (21)Ankle joint 128±1 (24) 117±1 (25) 130±1 (25) 126±1 (19) 141±1 (19) 30±1 (18)

Values are means ± s.e.m. (N = number of strides of valid data at this speed).

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Fig. 3. Representative limb joint angular trajectories during a stride, shown for the same elephant as in Fig. 2. Stance phase is shown in blue, swing phase inred.



During the stance phase of the forelimb (Table2; Fig.2), the upperarm was retracted throughout stance, along with the forearm (whichsometimes showed increasing segment angles very late in stance)and forefoot. The elbow and wrist joints both extended slightly,remaining almost static (but with hints of a shift from early flexionto extension in some strides), and then flexed late in stance (Fig.3).Similarly, decreasing segmental angles in stance [shifting to negative(i.e. behind vertical) angular values at lift-off] prevailed for thehindlimb. The thigh was protracted slightly before lift-off, the shankshowed a smooth rotation toward negative values throughout stance,whereas the hindfoot angle decreased steeply in late stance. Theknee joint flexed throughout stance (most steeply in late stance butwith a flexion–extension–flexion sequence in some strides) and theankle joint flexed past mid-stance, with some extension very earlyin stance in some strides, then extended in the last third of stance(Fig.3).

In earliest swing, segment angles continued to decrease (exceptfor the thigh), then slightly later reached their minimum angles(Fig.2), although more proximal segment angles tended to decreaselittle, or no further, from their lift-off values (0–3deg.; Table2).Segmental maximal swing angles occurred just before touch-downin the forelimb (angles decreasing gradually before touch-down)but closer to mid-swing in the hindlimb. Therefore, the segmentalangles began decreasing from late swing through touch-down, ratherthan initiating this decrease in early stance. However, the presenceof this late swing ‘retraction’ was more variable for the upper armand shank, especially at slower speeds. Elbow and wrist joint flexionduring swing (Fig.3; Table2) exceeded the values for the knee andankle (mean flexion of 20deg. and 24deg. from lift-off to minimalswing vs 12deg. and 4deg., respectively). The elbow and wrist jointsflexed and then extended steeply, beginning to shift back towardflexion in late swing. The knee joint flexed in early swing, thenextended for most of swing with a brief flexion before touch-down.The ankle joint was unusual in that it remained almost static (near

touch-down angle, with more gradual flexion in some strides) forthe last half of swing after an early swing extension–flexion shift(Fig.3).

The greatest ROM in the forelimb (Table2) was for the forefootsegment and wrist joint (90deg. and 66deg.), with smaller valuesfor more proximal segments and joints (36–52deg.). This is expectedas the rotations of proximal segments contribute to the rotation ofdistal segments. In the hindlimb, the pattern was similar; the hindfootsegment was the most mobile (76deg.), followed by the shank(55deg.) and thigh (29deg.), and the knee joint was slightly moremobile (42deg. ROM) than the ankle (30deg.). Overall, the upperarm segment was less vertical and had ~50% larger ROM than thethigh segment, during stance phase and across a whole stride; someof this presumably relates to scapular motion.

Effects of speed on limb motionAs the elephants increased their speed across an almost eightfoldspeed range, from the slowest speeds we recorded (0.62ms–1;Fr=0.026) to the fastest (4.92ms– 1; Fr=1.66), their segment andjoint motions mostly changed continuously. Relatively smallincreases of joint and segment rotation (Fig.4) and large changesof angular velocity (Fig. 5; discussed further below) relate toincreased stride length and especially frequency [i.e. decreases ofstance and swing time (Hutchinson et al., 2006)]. Movies 1 and 2in supplementary material show representative motion capture datain real time for added comparison. Many segments and joints didnot show significant changes of their angles with speed even fromslow walking to faster running. Shifts between joint flexion andextension during stance became more obvious in many trials athigher speeds (cf. Figs3 and 4; elbow, knee and ankle joint angles)but otherwise the sequence and timing of segment and joint motiondid not markedly change.

In the present study, for brevity, we describe the significantchanges from the slowest (û<0.25) to fastest (û>1.0) speeds (citing

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2742

mean values from Figs6–9; supplementary material Tables S1–S4),but these changes became evident at different speeds within thisrange for each segment/joint and event. Non-significant trends(~5deg. changes) existed for other cases, not outlined here (cf.Figs6–9).

Forelimb segmental angles changed most markedly with speed(Figs 4 and 6; supplementary material Table S1) for the upperarm segment at mid-stance (–15 deg.), the forearm segment atminimal (–7 deg.) and maximal (+8 deg.) swing, and the forefootsegment angle at lift-off (+10–15 deg.), minimal (–13 deg.) andmaximal (+21 deg.) swing. Joint angles reflected these changes(Fig. 6; supplementary material Table S2). At speeds past thepresumed gait transition point [(Ren and Hutchinson, 2008)û>0.50; speed range E–G in Fig. 6], notice that the trend formid-stance angles in particular became markedly steeper,indicating increased limb flexion, especially for the upper armand elbow.

In the hindlimb (Figs4 and 7; supplementary material TableS1),the thigh segment angle showed only moderate changes (7–8deg.),the shank angle decreased at mid-stance (–13deg.) and minimalswing (–5deg.), and the hindfoot angle only changed in swing phase:–16deg. for minimal swing and +14deg. for maximal swing.Overall, the knee joint exhibited marginally larger increases towardflexion, and greater ROM, than the elbow, whereas the wrist shiftedto become strikingly even more flexed during swing than the anklejoint, consistently with more than twice the ROM. By contrast,during stance, the ankle angle (changing from 116deg. to 108deg.)at mid-stance became even more flexed than the wrist angle(~186–189deg.). Again, at speeds past the presumed gait transitionpoint (û>0.50; speed range E–G in Fig.7), we observed steepertrends for thigh segment, knee joint and ankle joint mid-stance anglechanges with speed; the hindlimb was becoming appreciably moreflexed.

Joint and proximal segment angular velocities changed sharplywith increasing speed (Figs5, 8, 9; supplementary material TablesS3

and S4). Some noisy fluctuations are present but the data do showthe shifts of segment or joint angular velocities from positive tonegative values, especially during stance phase (e.g. elbow, kneeand ankle joints). The largest relative increases (as a multiple ofvalues at û<0.25 vs û>1.0) of angular velocity were during stance,often around 7–9� (but 203� for shank touch-down), comparedwith ~3� increases for swing-phase angular velocity and RAV.These changes concur with rapid decreases of stance (and swing)time in faster-moving elephants (Hutchinson et al., 2006). Thighsegment lift-off angular velocity showed the only shift of sign, froma mean value of 16degs–1 at the slowest speed to –17degs–1 at thefastest speed (Fig.9).

Unsurprisingly, the largest absolute increases of angular velocitywere for distal segments (supplementary material Table S3),especially RAV. Maximal swing velocity increases (positive values)were comparable for upper arm and thigh and for forearm and shank,but the increase in the forefoot was >50% larger than the increasein the hindfoot. There was a similar trend for velocity decrease –the largest decreases were for distal segments, but with comparablevalues among serially homologous segments (<–100 proximal,<–200 middle, >–300deg. s–1 distal). We measured very similartrends for the joints (Figs8 and 9; supplementary material TableS4).Few, if any, limb segment/joint angular velocity values seemed toplateau at faster speeds (Figs8 and 9; supplementary materialTablesS3 and S4). As stride frequency and swing time reach theirmaxima and minima at Fr>1.0 (Hutchinson et al., 2006), this isunsurprising; elephants at the top locomotor speeds measured in thepresent study (Fig.5; speed range G in Figs8 and 9) should havereached close to their peak angular velocities. At the fastest speeds,wrist joint angular velocity ranged from –772 to +773deg. s–1

whereas the ankle ranged from –180 to +390deg. s–1; the elbow andknee velocity ranges were more similar at –258 and +319deg. s–1

and –223 and +328 deg. s–1, respectively. Hence, overall, themaximal wrist RAV remained at least twice the RAV values of theother joints.

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Maximal vs utilized ROM in elephant jointsMaximal ROM values were 127, 115, 122 and 67deg. for the elbow,wrist, knee and ankle for the elephant (identical qualitative patternswere also observed in the adult elephant). We estimate that, duringhigh-speed locomotion, the more proximal joints used 31–40% oftheir available ROM whereas the more distal joints used 55–77%(Table3).

Body mass: relationship with limb motionElephants did not significantly change their limb segment or jointangles across the sevenfold size range we observed (P>0.05). Therewere slight statistical differences among sizes (supplementarymaterial TableS5), particularly <1000kg vs >3000kg, for the anglesof the forefoot segment at maximal swing, thigh segment at touch-down, shank segment at mid-stance and lift-off and knee joint atminimal swing. Yet only the forefoot, thigh, shank and knee joint’sminimal swing angles had consistent trends (slightly more extendedjoints in larger elephants) across the whole size range, and eventhese differences were slight. Total ROM also did not changesignificantly with size for any segments or joints (supplementarymaterial TableS5).

Segment and joint angular velocities decreased markedly withincreasing elephant size (Table4), as expected from measured size-

related differences in stride frequencies (Hutchinson et al., 2006).These reductions (most evident between <1000kg and >3000kganimals) occurred at different points in the stride for differentsegments and joints. Values for 1000–3000kg and >3000kg animalsdiffered only marginally.

For the forelimb, we measured angular velocity decreases withsize (toward zero values; supplementary material TableS5) for theupper arm at mid-stance and its RAV, the forearm at mid-stance,minimal and maximal swing and RAV; and the forefoot at maximalswing. No forelimb joints showed size-related decreases. For thehindlimb, angular velocity decreases were more widespread,occurring for the femur at mid-stance, maximal swing and RAV;the shank at all events except touchdown, and the hindfoot at mid-stance. In contrast to the forelimb, the knee joint showed largedecreases for lift-off, minimal and maximal swing and RAV,although the ankle joint merely reduced its mid-swing angularvelocity. Notably, touch-down angular velocity never showed astatistical size-related difference or clear trend for any segment orjoint.

African and Asian elephants: limb motion comparisonAs with general footfall patterns, we found some slight statisticaldifferences between limb segment and joint angles and angular

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velocities during normal walking in African and Asian elephants(supplementary material TablesS6 and S7). We detected a fewstatistically significant differences for the angular velocities of twosegments and one joint: the forearm segment at minimal swing,forefoot segment at minimal swing and RAV, and knee joint atminimal swing (supplementary material Table S7). The meandifferences (African minus Asian angular velocity values) were–25deg. s–1 (25% of African value), 99deg. s– 1 (26%), 116deg. s –1

(15%) and –39deg. s –1 (31%), respectively.

DISCUSSIONIn this section, we scrutinize how well the stereotype of a columnarposture applies to elephants (i.e. how vertical are their limbs?),examine how much of their maximal range of motion elephant jointsuse during running (and relate these values to estimates for otherspecies), compare and integrate our results with those of previousstudies, discuss whether elephants show appreciable size or speciesdifferences in limb motions and, finally, consider how similar ordifferent elephant limb motion is to published data for other species.

Limb motion: how columnar are elephants?Considering other studies of footfall patterns (Hutchinson et al.,2006) and evidence for bouncing gaits at higher speeds (Hutchinson

et al., 2003; Ren and Hutchinson, 2008), our results are changinghow elephants are viewed: no longer simply the straight-limbed,inflexible juggernauts of classical literature. The present study showsthat elephant limbs are more than just columnar legs for necessity,not for flexure. Flexion increases gradually with speed (Fig.10), sothe posture of an elephant at top speed is somewhat different froma slow-walking elephant – there is no single columnar postureadopted at all speeds. A fully columnar limb would incur large,potentially damaging, transient impact forces and jarring, expensivecenter of mass motions due to its infinite stiffness (Fischer andBlickhan, 2006).

Few joints or segments are very columnar during stance (let aloneswing); the limbs appear vertical but the underlying skeleton is onlypartly so (Fig.10). In particular, during stance, the upper arm, shankand hindfoot segments remain at >20deg. angles to the vertical,even during slow walking. Only the wrist joint behaves as a relativelystatic (i.e. with little motion) structure during stance; others maintainangles of <160deg. and exhibit stronger flexion or extensionmotions. Furthermore, there are marked differences between limbsand joints (Gambaryan, 1974; Hildebrand, 1984; Hildebrand andHurley, 1985); for example, in swing phase the wrist and knee jointsmove through moderate ROM arcs (89deg. and 49deg., respectively,vs <40deg. for other joints/segments).

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Our study refutes the notion that elephants have ‘inflexible’ or‘rigid’ ankles (Gambaryan, 1974; Hildebrand, 1984; Hildebrand andHurley, 1985; Paul, 1998). The ankle ROM (mean 37deg. vs 89deg.)and peak angular velocities (mean –180/+390degs–1 vs–772/+773degs–1 in ankle vs wrist) are less than half those of thewrist [not less than one-fifth as in Hildebrand (Hildebrand, 1984)]even at Fr>1 but the movement is appreciable and not purely passive(but see Gambaryan, 1974). For example, ~27deg. of ankledorsiflexion occurs during swing, which is likely to be activelycontrolled in order to achieve ground clearance. As the ankledorsiflexes and rebounds 15–20deg. during stance in running, andextensive elastic tissues cross the ankle joint (Gambaryan, 1974), thereis the potential for elastic energy storage – it is probably incorrect tocharacterize elephants as having ankles that are not spring-like (Paul,1998). Although the wrist uses a large ROM during swing phase, itsstance phase motion is actually less spring-like than that of the ankle.Unlike plantigrade primates (Pike and Alexander, 2002) or digitigradefelids (Day and Jayne, 2007), elephants do not hold their ankles (orknees in the additional case of felids) relatively static throughout thestride; the ankle is a dynamic structure. However, our in vitro study(see below) of elephant joint ROM shows that elephant ankles havelow mobility relative to cats, dogs and horses (but not humans), whichmay simply correlate with their increased plantigrady, a speculationthat deserves testing with data from other species.

A brief mention of the patterns of the segment/joint abductionand adduction we observed during locomotion in elephants iswarranted here as, despite their size and graviportal, fairly uprightlimb structure, they clearly do use appreciable non-sagittal limbmotions (see also Schwerda, 2003) that are obfuscated by labelslike ‘columnar’. Although our markers were positioned lateral tojoint centers and hence would generally lead to quantitativeoverestimates of abduction that are unreliable, we can safely inferqualitative patterns of motion orthogonal to flexion/extensionmotions that can apply to all speeds, sizes and species observed.Elephants smoothly adducted their upper arm and thigh from mid-swing through late-stance phase, then abducted. The elbow tendedto be fairly static in adduction during stance, then abducted andadducted in swing, whereas the knee showed a similar motion tothe upper arm and thigh but with markedly large swing-phaseabduction [note that the knee joint’s helical axis passively contributesto this motion (Weissengruber et al., 2006)]. The wrist remainedquite static (more so than the elbow) in slight abduction during stance(much like its stasis in extension) and then quickly abducted, thenadducted during swing. The ankle adducted throughout stance thenabducted in late swing after being static in early swing. Overall, themagnitudes of swing phase abduction in the hindlimb tended to bemarkedly larger than those of the forelimb. Like Schwerda(Schwerda, 2003), we infer that elephants achieve foot-ground

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clearance during swing largely via flexion of the wrist (which ismuch greater than ankle flexion) and abduction of the wholehindlimb (especially hip and knee). Thus, elephant limbs are oftennot as parasagittal as might be assumed.

We have also found that the ‘columar, graviportal vs crouched,cursorial’ dichotomy also breaks down somewhat when othermammalian species, large and small, cursorial and not, are comparedwith elephants (see further below). Surprisingly, the columnar,graviportal limbs of elephants and the flexed, cursorial limbs ofhorses are posed rather similarly at comparable speeds, exceptingdifferences in foot posture (Dutto et al., 2006; Marey and Pagès,1887), a similarity that many functional studies have overlooked(see below). We feel that the differences between cursorial andgraviportal limb structure and function have often been overstated– both are common in larger land animals and both tend to involvemore straightened limbs as a size-related consequence (Biewener,1989), along with other features (Coombs, 1978).

Joint ranges of motion: how ʻoverdesignedʼ are elephantjoints for locomotion?

Our results for elephant and joint ROM (Table 3) reject the nullhypothesis that all joints use a similar fraction of their maximalROM, as the amount of maximal ROM actually used in running(Fr>1) varies from 31 to 77%. Alternatively, perhaps more distal

joints (wrists and ankles) of elephant limbs use a larger fractionof their maximal range of motion than more proximal joints(elbows and knees). This could be because, as in many animals,more distal joints of elephants use a wider absolute range ofmotion, presumably related to their lower segmental inertia(Gambaryan, 1974; Hildebrand, 1984; Hildebrand and Hurley,1985; Marey and Pagès, 1887). This hypothesis is tentativelysupported (Table 3).

A second alternative hypothesis is that, for reasons of safety,perhaps larger animals such as elephants stay far from their limitsof joint motion (i.e. show positive allometry of the maximal ROMvs utilized ROM ratio). Few published data on maximal joint ROMin vivo and in vitro exist for other mammalian species that woulddraw elephants into such a broader context, but Table3 showscomparative data for cats, dogs, humans, horses and elephants(~4–4000kg body mass). These data do not fit the ideal criteria ofbeing drawn from the same individuals/breeds using identicalmethods (except for the elephant and horse methodology) andtherefore demand careful interpretation. We infer that theproximal–distal decline of joint ROM found for elephants is notubiquitous for all species but at least applies to elephants, horsesand humans. Yet interestingly, for all species, the elbow and kneejoints show more narrowly bounded (31–50% and 32–45%,respectively) percent usages of ROM, so the null hypothesis of there

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Table 3. Limb joint maximal ROM, maximal in vivo ROM in a running stride (Fr~1; trotting for cat, dog and horse) and percentage of maximalROM used in running

Species

Joint Cat Dog Human Horse Elephant

Maximal ROM of jointselbow 142.5 145 143 120±0.89 127±1.4wrist 170 182.6 151 147±1.4 115±3.2knee 160 140 145 127±1.7 122±0.28ankle 177 170 69 122±0.43 67±1.7

ROM in vivoelbow 60 52.5 n/a 60 40±1wrist 75 110 n/a 89.5 89±2knee 51 55 65 45.9 49±1ankle 51 35 50 53.3 37±1

% Maximal ROM usedelbow 0.42 0.36 n/a 0.50 0.31wrist 0.44 0.60 n/a 0.61 0.77knee 0.32 0.39 0.45 0.36 0.40ankle 0.29 0.21 0.72 0.44 0.55

Values are means ± s.e.m. (for horse and elephant data) where available. Non-elephant maximal range of motion (ROM) and running ROM data are fromdomestic cats (Goslow et al., 1973; Miller and van der Meche, 1975; Newton and Nunamaker, 1985), domestic dogs (DeCamp et al., 1993; Newton andNunamaker, 1985), fit male humans (Boone and Azen, 1979; Novacheck, 1998) and Dutch Warmblood horses (present study; Back et al., 1995a; Back etal., 1995b). As data for maximal ROM in cats, dogs and humans were not from defleshed cadavers, these numbers are probably slightly underestimated,leading to slight overestimates of % maximal ROM used for these species. Human forelimb in vivo values are not applicable (n/a) for comparison withrunning quadrupeds. ROM in vivo data for galloping/sprinting would generally be slightly larger.

Table 4. Limb segment and joint angular velocity (deg.s1) data of both species at different body mass ranges, during walking (û =0.25–0.50)

Stance Swing

Joint or segment Body mass Touch-down Mid-stance Lift-off Min. Max. RAV

ForelimbUpper arm <1000 kg –61±10a –60±3a –12±3a –77±9a 135±6a 232±11a

1000–3000 kg –33±8a –45±3a,b –7±6a –36±7a 121±8a 196±13a,b

>3000 kg –30±9a –42±3b –25±5a –48±7a 124±3a 204±7b

Forearm <1000 kg –45±7a –67±3a 70±8a –128±7a 224±12a 344±13a

1000–3000 kg –48±4a –57±3b 78±11a –104±8b 197±9a 312±12a

>3000 kg –47±4a –50±1c 66±8a –92±2b 168±3b 266±4b

Forefoot <1000 kg –93±9a –51±3a –305±10a –316±16a 442±12a 759±26a

1000–3000 kg –76±17a –36±2a –233±28a –232±34a 410±36a,b 699±75a

>3000 kg –91±7a –33±2a –285±20a –341±11a 364±9b 710±18a

Elbow joint <1000 kg –14±14a 9±3a –80±7a –144±6a 213±16a 357±17a

1000–3000 kg 26±13a 13±4a –89±13a –140±9a 152±9a 303±14a

>3000 kg 15±14a 6±3a –64±12a –141±9a 147±7a 294±11a

Wrist joint <1000 kg –60±12a 16±2a 375±13a –428±14a 387±15a 816±25a

10003000 kg –44±14a 21±2a –326±30a –335±44a 342±23a 744±84a

>3000 kg –44±6a 17±2a –351±28a –458±13a 332±11a 793±22a

HindlimbThigh <1000 kg –37±3a –68±4a 39±5a –37±4a 140±6a 233±8a

1000–3000 kg –36±4a –33±7b 60±5a –35±3a 97±4b 166±10b

>3000 kg –28±1a –42±2b 29±5a –33±2a 89±2b 146±4b

Shank <1000 kg –48±9a –80±5a –97±4a –101±4a 223±7a 343±11a

1000–3000 kg –39±4a –49±10b –53±4b –73±5b 193±4a,b 290±8a,b

>3000 kg –37±3a –61±2a,b –57±3b –70±3b 186±5b 270±6b

Hindfoot <1000 kg –68±17a –57±3a –250±16a –305±7a 289±10a 594±14a

10003000 kg –86±10a –32±6b –260±13a –249±17a 277±15a 598±21a

>3000 kg –86±6a –33±2b –285±13a –308±8a 245±6a 558±9a

Knee joint <1000 kg –10±10a –12±7a –136±8a –202±5a 174±7a 376±10a

1000–3000 kg –2±6a –16±4a –115±8a,b –128±7b 154±4a,b 289±9b

>3000 kg –8±4a –19±2a –86±5b –122±5b 149±4b 269±8b

Ankle joint <1000 kg 21±15a –22±4a 153±13a –137±10a 220±9a 357±17a

10003000 kg 48±12a –17±4a 207±13a –120±11a,b 191±15a 377±14a

>3000 kg 49±7a –28±1a 227±13a –99±5b 252±9a 360±11a

Values are means ± s.e.m. Identical letters indicate body mass groups within a column that do not differ significantly from each other (P>0.05); angular velocityvalues that are significantly slower for larger elephants (at this speed) are emphasized in bold. RAV=range of angular velocities (maximal – minimal).


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being no difference among joints may roughly apply to somehomologous joints. There is a general trend for maximum possiblejoint ROM to decline with size, except for the ankle joint, which issimilar in humans and elephants and strikingly different from othertaxa including horses (Table3). However, no clear scaling trend isevident for the percentage of maximal ROM used amonghomologous joints. Hence, the second alternative hypothesis is notsupported.

The method used in the present study was limited in that we didnot apply massive elephantine loads to the cadaveric material, whichwould provide an extra amount of flexion and extension. However,we felt that we were reaching reasonable approximations of maximalROM as the joint ligaments and capsules seemed to be approachingtheir limits of failure. It is likely that elephants employ larger jointROM during non-locomotor activities such as lying down, so thebehavioral (not to mention mechanical, such as tissue stress andstrain) context of ROM usage in animals remains a fertile groundfor exploration, and the ROM of the scapula and shoulder/hip jointsdeserve investigation. We hope that this preliminary investigationof joint ROM inspires researchers to investigate this phenomenonin other species, which may reveal general principles of joint designand control.

Comparisons with previous studiesOur limb motion data (using our mean values for Fr>1.0) concurwith those from previous studies of Asian (Gambaryan, 1974; Mareyand Pagès, 1887) and African (Alexander et al., 1979b; Hildebrandand Hurley, 1985) elephant limb motions during running. However,the lack of data on marker placement and other methods, speed,size or other parameters makes comparison difficult; differences of10–15deg. are expected and evident among studies. The closestmatch among all studies is for thigh segment motion.

Overall, the results from the present study compare least wellwith Hildebrand and Hurley’s study (Hildebrand and Hurley, 1985)and better with others (cited above). The former study (see alsoHildebrand, 1984) showed a less vertical upper arm segment andless extended wrist, knee and ankle joints, often with disagreement

of 30–50deg. with measurements observed in other studies. Jointcenter estimation surely contributed to some differences, especiallyfor the toe ‘marker’ this was positioned more laterally at midfootrather than cranially on digit 3.

Two studies (Gambaryan, 1974; Hildebrand and Hurley, 1985)found much higher wrist ROM compared with our mean values(152deg. and 104deg., respectively, vs 89deg.; the second valuewas observed in some of our faster individuals). Gambaryan’s valuewas clearly a miscalculation [cf. fig.113 and table11 in Gambaryan(Gambaryan, 1974); total ROM in the former is ~85deg.]. Our anglestended to be the most flexed of those observed, especially at mid-stance, although the figured angles of Marey and Pagès (speedunknown) and Alexander et al. (Fr>1.0) are generally similar(Alexander et al., 1979b; Marey and Pagès, 1887). Aside from thedifferences already noted, ROM is generally larger in Gambaryan’sstudy (we only found a much larger ROM in swing vs stance phasefor the elbow, wrist and knee) but is otherwise roughly in agreementamong studies, as are the typical patterns of flexion and extension.

We concur with Gambaryan that the more proximal segments ofelephants (upper arm and thigh) switch between flexion andextension (or vice versa) twice per stride (using angular displacementto identify switches; Figs2– 4), whereas more distal joints typicallyswitch four times (‘biphasic’ motion) (Gambaryan, 1974). Abiomechanical or control-based explanation for these patternsremains elusive, and unfortunately angular velocity data are too noisy(Fig.5) to provide deeper insight. In the present study, we havepresented the first data on segment/joint angular velocities forelephants, although Hildebrand and Hurley used unspecified values(for an animal traveling at an unsubstantiated speed of 10ms–1) tocalculate mechanical energies of the limb segments (Hildebrand andHurley, 1985). Our finding for the wrist joint’s rapid flexion andextension (>720 deg. s–1) is exceptional but other joints (evenproximal segments) showed in our data peak rotations of>200deg. s–1.

Like footfall patterns (Hutchinson et al., 2006) and center ofmass mechanics (Ren and Hutchinson, 2008), elephant limbmotion changes almost continuously with speed. Differences are

L. Ren and others

ForelimbHindlimb

gniwSecnatSgniwSecnatS

Slow

Fast

Fig. 10. Stick figure portrayals of elephant limb motions for subject O (Table 1) in both stance and swing phases for the fore- and hindlimbs at normalwalking (1.26 m s–1; Fr=0.11; shown at 20 Hz), and fast running (4.81 m s–1; Fr=1.56; shown at 40 Hz). Because of space constraints the hip and shoulderpositions are kept constant during the swing phase. Also represented as online supplementary material (Movies 1 and 2).



evident at the extremes (Hutchinson et al., 2003), but thoseextremes lie on a continuum. Our data show that the majorchanges of elephant limb motion with increasing speed aretemporal (i.e. angular velocities; Figs 5, 8, 9). Likewise the slightincreases of joint angular motions with speed we have measuredwould generate the observed stride length increases with speed(Hutchinson et al., 2006). The elongate limbs of elephants(Alexander et al., 1979a) allow even small increases of rotationalarcs to contribute substantially to increasing stride length and thusspeed. For example, proximal segments will still contribute themost to increasing step length – estimated stance phase scapularmotion for walking elephants is 15±5 deg., contributing 55% ofstep length (Fischer and Blickhan, 2006; Schwerda, 2003); thighmotion is 23±1 deg. (our data), contributing up to 82% of steplength (Fischer and Blickhan, 2006; Schwerda, 2003). However,measurements of these proximal segment and joint motions willstill require advanced methodology that carefully takes intoaccount the larger relative skin motions that are expected to occurproximally (Back et al., 1995a; Back et al., 1995b; Leardini etal., 2005; Reinschmidt et al., 1997; van Weeren et al., 1988; vanWeeren et al., 1990). Rather than present flawed kinematic datafor these motions, we prefer to accept the limitations of thisstudy caused by excluding them and await more accuratemeasurements.

The observed increase of limb flexion (especially at mid-stance,particularly past û=0.50; Figs6 and 7) with speed is consistent withthe hypothesis that elephants shift to bouncing gaits (Hutchinson etal., 2003; Ren and Hutchinson, 2008) and are, in a sense, ‘Groucho

running’ (McMahon et al., 1987). The hindlimbs (generally moreflexed than the forelimbs) have already been inferred to involvesome bouncing at moderate speeds (Ren and Hutchinson, 2008).Yet, as even the forelimbs became more flexed at the fastest speedswe observed (Fr>1.0), this leaves open the possibility that there arebouncing forelimb mechanics at such speeds. Fig. 10 andsupplementary material Movies 1 and 2 summarize the moderatechanges of limb motion with speed. In particular, a flattening of thehip (and shoulder) arc of motion during stance is evident (Fig.10),although this motion is less concave in the trial shown thandescribed for other elephants (Hutchinson et al., 2003; Hutchinsonet al., 2006).

Although our fastest speed data (4.92ms–1; Fr=1.66) are not asspeedy as the near-maximal documented velocities for athleticelephants (6.8ms–1; Fr>2.5) (Hutchinson et al., 2006), our data (e.g.Figs6–9) could be extrapolated to estimate kinematics at greaterspeeds, with the caveat that at these speeds stride frequency isprobably already at its maximum, and hence increased joint angularexcursions, rather than velocities, should play a larger role in speedincrease (Hutchinson et al., 2006).

Size and species differences between elephantsWe found no major differences between the motions of smaller andlarger elephants, except for the lower angular velocities reached bymany segments and joints in larger elephants (Table4), and soconclude that there are no biologically significant size-relateddifferences in elephant limb kinematics. This concurs withintraspecific data for other animals (e.g. Pennycuick, 1975), unlikebroad interspecific scaling trends for other species (Biewener, 1989;Biewener, 1990; but see Day and Jayne, 2007). Likewise, as thedifferences between African and Asian elephants are so relativelysmall (supplementary material TablesS6 and S7), we conclude thatno profound biological differences exist for their locomotordynamics (Hutchinson et al., 2006; Ren and Hutchinson, 2008).

Our conclusions should apply well to other members of theelephantid crown group such as mammoths, at least where limbproportions (Pike and Alexander, 2002) and other aspects oflocomotor morphology overlap with extant elephants (e.g.Christiansen, 2007). Even small dwarf elephants may not havediffered in posture from extant elephants, although there istantalizing anatomical evidence that this may not be the case (Roth,1992). Yet, because some elephantids reached masses of >10,000kg(Christiansen, 2004), biomechanical constraints might have imposedmore severe limits on limb angles and ROM [see Hutchinson et al.(Hutchinson et al., 2006) for examples of intraspecific locomotorscaling].

Comparison with other speciesHow different are elephant limb motions from bipedal, smaller, lesslong-legged or more cursorial animals? As humans have a similarhindlimb design to elephants (Weissengruber et al., 2006) (e.g. longfemur and short tibia, large functionally plantigrade foot) despitetheir bipedalism, it is interesting to compare their limb motions.These were previously described as quite similar, except for thedamping, compressive and more digitigrade feet of elephants andslightly greater limb flexion of humans (Marey and Pagès, 1887).Otherwise, the patterns compare well (Fig.11). Elephants alsoexhibit similar total limb protraction and retraction angles to humans[~22deg. (Novacheck, 1998; Schwerda, 2003; Seyfarth et al.,2003)]. The main differences we find are the smoother motions[attributed by Gambaryan (Gambaryan, 1974) to fascial sheets] andsmaller ROM of elephant limbs. Even the foot motions of elephants

–25

0

25

50

–80

–40

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dlim

b se

gmen

t ang

le (

deg.

)

Proportion of stride cycle (%)

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Foot

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Fig. 11. Comparison of hindlimb segment/joint kinematics between humansand elephants. Elephant hindlimb data shown are for subject N (Table 1)fast walking at 1.93±0.07 m s–1 (Fr=0.25; N=2) and human limb data shownare from Ren et al. [(Ren et al., in review) age 28 years, mass 69 kg];walking at 1.45±0.08 m s–1 (Fr=0.25).


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and humans are similar (especially in stance), despite someanatomical differences, although the more horizontally oriented feetof humans indicate some differences, at least in relative jointmoments.

Elephant stance phase segmental and joint ranges of motion arealso surprisingly similar to those observed in trotting horses[3–4ms–1 (Back et al., 1995a; Back et al., 1995b; Dutto et al., 2006)],although toe joint motions in elephants remain unknown [cf.Figs2–4, 10 and figs3 and 4 in Dutto et al. (Dutto et al., 2006)].Elephants also have more flexed ankles and more extended wristjoints than horses. This fundamental similarity was recognized longago (Marey and Pagès, 1887) but has since been largely forgottenby comparative analyses. Knee flexion in elephants exceeds that introtting horses. Horses can thus be only marginally less columnarthan elephants and even more columnar for some joints (e.g. ankle,knee). Our in vitro analysis also shows similar maximal joint ROMfor the elbow and knee in horses and elephants, among othersimilarities (Table3). This evidence has been overlooked by manyprevious qualitative studies of functional anatomy and thecursorial–graviportal continuum (e.g. Bakker, 1986; Gregory, 1912;Gambaryan, 1974; Hildebrand, 1984; Paul, 1998; Paul andChristiansen, 2000).

In many ways, limb motion in elephants is typical of walking,and even running, in smaller quadrupedal mammals. As widelyrecognized, elephants generally adopt straighter limbs but their limbsstill use poses and ROM that are similar, or identical, to those ofsmaller animals, not just humans and horses. The ROM of elephantlimbs (particularly in swing phase but also in stance) overlaps theROM used even by many small mammals, although the ROM ofelephants can be smaller than some values in much smaller cursorialtaxa (e.g. Day and Jayne, 2007). For example, in the stance phaseof walking, elephants and many other mammals retract their thighsegment or extend their hip joint across an arc of 20–40deg. andflex the knee through ~25–50deg., with similar values for theforelimb, although elephants flex their elbows and ankles throughsmaller arcs during stance (9 deg. and 12 deg. vs 30–40 deg.)(Table2; Figs3 and 4) (Fischer et al., 2002; Pike and Alexander,2002). The rather static stance-phase patterns of the elbow andespecially wrist joints of elephants are also observed in trottinghorses [wrist (Back et al., 1995a)], dogs [elbow (De Camp et al.,1993)] and, at least, walking felids [wrist in particular (Day andJayne, 2007)]. As such stasis is less evident in smaller mammals(Fischer et al., 2002) it is tempting to speculate that it relates to amore vertical limb orientation, cursoriality–graviportality and bodysize.

Like many other mammals, elephants use late swing-phase limbretraction at all speeds (Day and Jayne, 2007; Fischer et al., 2002),unlike humans who only use it during running. This allows limbprotraction to be modulated at touch-down in response to locomotorperturbations, contributing to stability (Seyfarth et al., 2003).Hildebrand and Hurley contended that elephants do not exhibitsegmental retraction after lift-off or just before touch-down(Hildebrand and Hurley, 1985), but these patterns indeed wereevident in our elephants, even at slower speeds [except where notedin the Results; also see figs115 and 116 in Gambaryan (Gambaryan,1974)].

Elephants change their limb motions moderately with speed,unlike many smaller mammals (Fischer et al., 2002). As in othermoderately-large mammals (Gambaryan, 1974), elephants usesomewhat less biphasic distal joint motion (flexion-extensionswitches; see above) during stance [cf. fig. 5 in Pike and Alexander(Pike and Alexander, 2002) for Perissodactyla and Artiodactyla; Day

and Jayne (Day and Jayne, 2007) for felids] than in smallermammals (e.g. Fischer et al., 2002). The simpler flexion and then~50deg. extension of the knee during swing most resembles thatobserved in some Carnivora [(Day and Jayne, 2007) see fig.5 inPike and Alexander (Pike and Alexander, 2002)].

CONCLUSIONSWe have compiled a large dataset of 288 strides from 15 elephantsof both major extant species, covering a sevenfold size range andan eightfold speed range. We hope that our analysis of skin-markerplacement, and caution about skin motion errors (e.g. scapula,shoulder and hip motion), stimulates further progress for othercomparative studies, which have lagged behind progress on humanand horse skin motion artefacts (e.g. Back et al., 1995a; Back et al.,1995b; Cappozzo et al., 1996; Filipe et al., 2006; Fischer et al.,2002; Leardini et al., 2005; Reinschmidt et al., 1997; van Weerenet al., 1988; van Weeren et al., 1990; but see Gatesy, 1999; Rubensonet al., 2007). Here we have shown that elephant limb motions: (1)do not simply involve a vertical (or parasagittal) columnar posture[‘mobile Doric columns’; p. 214 in Bakker (Bakker, 1986)] – limbmotion changes gradually with speed, and some joints are quiteflexed during stance, showing potential for elastic energy storageeven in the purportedly inflexible ankle; (2) exhibit appreciabledifferences within and between limbs – the wrist has roughly doublethe range of motion and peak angular velocities of the ankle, yetthe wrist is quite static during stance whereas the knee is the mostmobile joint in the hindlimb; (3) have a general proximal distalincrease in how much of maximal ROM is used at faster speeds (asin, at least, humans and horses); (4) contribute to speed changesmainly via angular velocity, which can be quite large (>720degs1

in flexion and extension for the wrist), although an increased ROMoccurs for some segments and joints; (5) reduce their angularvelocity as size increases but otherwise do not change; (6) areessentially identical for African and Asian species despite someanatomical differences; and finally (7) are more similar to those ofsmaller mammals than has previously been acknowledged. Elephantlimbs have a more limited ROM for some segments/joints and are,of course, more straight-legged on average – but barely so relativeto walking humans or especially to trotting horses. Elephant limbmotions fall on a continuum that does not dichotomize neatly into‘flexed, cursorial’ and ‘columnar, graviportal’ categories. To acertain extent, the term columnar obscures more information aboutelephant locomotion than it conveys and, as such, is sometimes nota useful term in light of modern understanding of locomotordynamics. The limb motions of running horses are mostly onlytrivially less columnar than those of elephants or are actually morecolumnar for some distal joints. These data demonstrate that limbconfiguration and running ability [top speeds <20ms–1 in horses,~7ms–1 in elephants (Hutchinson et al., 2006)] are not as tightlyassociated as sometimes assumed (e.g. Bakker, 1986; Paul, 1998;Paul and Christiansen, 2000). The data provided are useful not onlyin the comparative context emphasized here, but also for futurestudies of locomotor mechanics and as baseline data for clinicalgait analysis of elephants.

LIST OF ABBREVIATIONSFr Froude number h hip heightg acceleration due to gravity RAV range of angular velocity ROM range of motion v velocityû dimensionless speed (Fr0.5)

L. Ren and others



For their expert assistance with elephants we thank Anthony Tropeano and staff(Colchester Zoo, UK), Andrew Plum and staff (West Midlands Safari Park, UK),Lee Sambrook and staff (Whipsnade Wild Animal Park, UK), Thüringer ZooparkEhrfuhrt (Germany) staff, and Richard Lair and the staff of the Thai ElephantConservation Centre (Thailand) and Forest Industry Organization. We thank KarinJespers for her assistance with Qualisys data collection in the UK, as well asDaniel Seng (Qualisys, Inc.) and Thanasit Ujjin (United Sports Trading Pvt, Ltd.)for assistance in Thailand. Advice on statistical analyses was kindly provided byRenate Weller and Zhangrui Cheng. J.R.H. thanks the BBSRC for NewInvestigator research grant number BB/C516844/1 awarded in 2005, and theDepartment of Veterinary Basic Sciences (The Royal Veterinary College) forfinancial support. Hearty thanks for constructive input on this work are due toSteve Gatesy and three anonymous reviewers. Aid with conducting the Thailanddata collection was provided by Norman Heglund, Patrick Willem, GiovanniCavagna, Joakim Genin and others.

REFERENCESAlexander, R. McN. and Jayes, A. S. (1983). A dynamic similarity hypothesis for the

gaits of quadrupedal mammals. J. Zool. 201, 135-152.Alexander, R. McN., Jayes, A. S., Maloiy, G. M. O. and Wathuta, E. M. (1979a).

Allometry of the limb bones of mammals from shrews (Sorex) to elephant(Loxodonta). J. Zool. 187, 305-314.

Alexander, R. McN., Maloiy, G. M. O., Hunter, B., Jayes, A. S. and Nturibi, J.(1979b). Mechanical stresses in fast locomotion of buffalo (Syncerus caffer) andelephant (Loxodonta africana). J. Zool. 189, 135-144.

Back, W., Schamhardt, H. C., Savelberg, H. H. C. M., van den Bogert, A. J., Bruin,G., Hartman, W. and Barneveld, A. (1995a). How the horse moves: 1. Significanceof graphical representations of equine forelimb kinematics. Equine Vet. J. 27, 31-38.

Back, W., Schamhardt, H. C., Savelberg, H. H. C. M., van den Bogert, A. J., Bruin,G., Hartman, W. and Barneveld, A. (1995b). How the horse moves: 2. Significanceof graphical representations of equine hind limb kinematics. Equine Vet. J. 27, 39-45.

Bakker, R. T. (1986). Dinosaur Heresies. New York: William Morrow.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.Boone, D. C. and Azen, S. P. (1979). Normal range of motion in male subjects. J.

Bone Joint Surg. 61-A, 756-759.Cappozzo, A., Catani, F., Leardini, A., Benedetti, M. and Della Croce, U. (1996).

Position and orientation in space of bones during movement: experimental artifacts.Clin. Biomech. 11, 90-100.

Cappozzo, A., Della Croce, U., Leardini, A. and Chiari, L. (2005). Human movementanalysis using stereophotogrammetry Part 1, theoretical background. Gait Posture21, 186-196.

Christiansen, P. (2004). Body size in proboscideans, with notes on elephantmetabolism. Zool. J. Linn. Soc. 140, 523-549.

Christiansen, P. (2007). Long-bone geometry in columnar-limbed animals: allometry ofthe proboscidean appendicular skeleton. Zool. J. Linn. Soc. 149, 423-436.

Coombs, W. P. (1978). Theoretical aspects of cursorial adaptations in dinosaurs. Q.Rev. Biol. 53, 393-417.

Csuti, B. A., Sargent, E. L. and Bechert, U. S. (2001). The Elephantʼs Foot: Careand Prevention of Foot Conditions in Captive Asian and African Elephants. Ames:Iowa State Press.

Day, L. M. and Jayne, B. C. (2007). Interspecific scaling of the morphology andposture of the limbs during the locomotion of cats (Felidae). J. Exp. Biol. 210, 642-654.

DeCamp, C. E., Soutas-Little, R. W., Hauptman, J., Olivier, B., Braden, T. andWalton, A. (1993). Kinematic gait analysis of the trot in healthly Greyhounds. Am. J.Vet. Res. 54, 627-634.

Dutto, D. J., Hoyt, D. F., Clayton, H. M., Cogger, E. A. and Wickler, S. J. (2006).Joint work and power for both the forelimb and hindlimb during trotting in the horse.J. Exp. Biol. 209, 3990-3999.

Egger, G. F., Witter, K., Weissengruber, G. and Forstenpointner, G. (2008).Articular cartilage in the knee joint of the African elephant, Loxodonta africana,Blumenbach 1797. J. Morphol. 269, 118-127.

Filipe, V. M., Pereria, J. E., Costa, L. M., Mauricio, A. C., Couto, P. A., Melo-Pinto, P. and Varejao, A. S. P. (2006). Effect of skin movement on the analysis ofhindlimb kinematics during treadmill locomotion in rats. J. Neurosci. Methods 153,55-61.

Fischer, M. S. and Blickhan, R. (2006). The tri-segmented limb of therian mammals:kinematics, dynamics, and self-stabilization – a review. J. Exp. Zool. 305A, 935-952.

Fischer, M. S., Schilliug, N., Schmidt, M., Haarhaus, D. and Witte, H. (2002). Basiclimb kinematics of small therian mammals. J. Exp. Biol. 205, 1315-1338.

Gambaryan, P. P. (1974). How Mammals Run. New York: John Wiley and Sons.Gatesy, S. M. (1999). Guineafowl hind limb function. I: Cineradiographic analysis and

speed effects. J. Morphol. 240, 115-125.Goslow, G. E., Reinking, R. M. and Stuart, D. G. (1973). The cat step cycle: hind

limb joint angles and muscle lengths during unrestrained locomotion. J. Morphol.141, 1-42.

Gregory, W. K. (1912). Notes on the principles of quadrupedal locomotion and themechanisms of the limbs in hoofed animals. Ann. N. Y. Acad. Sci. 22, 267-292.

Hildebrand, M. (1984). Rotations of the leg segments of three fast-running cursorsand an elephant. J. Mammal. 65, 718-720.

Hildebrand, M. and Hurley, J. P. (1985). Energy of the oscillating legs of a fast-moving cheetah, pronghorn, jackrabbit, and elephant. J. Morphol. 184, 23-31.

Hutchinson, J. R., Famini, D., Lair, R. and Kram, R. (2003). Biomechanics: are fast-moving elephants really running? Nature 422, 493-494.

Hutchinson, J. R., Schwerda, D., Famini¸, D., Dale, R. H. I., Fischer, M. and Kram,R. (2006). The locomotor kinematics of African and Asian elephants: changes withspeed and size. J. Exp. Biol. 209, 3812-3827.

Hutchinson, J. R., Miller, C. E., Fritsch, G. and Hildebrandt, T. (2008). Theanatomical foundation for multidisciplinary studies of animal limb function: examplesfrom dinosaur and elephant limb imaging studies. In Anatomical Imaging: Towards aNew Morphology (ed. H. Endo and R. Frey), pp. 23-38. Tokyo: Springer-Verlag.

Laws, R. M., Parker, I. S. C. and Johnstone, R. C. B. (1975). Elephants and TheirHabitats. The Ecology of Elephants in North Bunyoro, Uganda. Oxford: ClarendonPress.

Leardini, A., Chiari, L., Della Croce, U. and Cappozzo, A. (2005). Human movementanalysis using stereophotogrammetry part 3, soft tissue artifact assessment andcompensation. Gait Posture 21, 212-225.

Marey, E. J. and Pagès, C. (1887). Locomotion comparèe: mouvement du membrepelvien chez lʼhomme, lʼéléphant et le cheval. C. R. Acad. Sci. 105, 149-156.

McMahon, T. A., Valiant, G. and Frederick, E. C. (1987). Groucho running. J. Appl.Physiol. 62, 2326-2337.

Miller, C. M., Basu, C., Fritsch, G., Hildebrandt, T. and Hutchinson, J. R. (2008).Ontogenetic scaling of foot musculoskeletal anatomy in elephants. J. R. Soc.Interface 5, 465-476.

Miller, S. and van der Meche, F. G. A. (1975). Movements of the forelimbs of the catduring stepping on a treadmill. Brain Res. 91, 255-269.

Newton, C. D. and Nunamaker, D. M. (1985). Textbook of Small AnimalOrthopaedics. Philadelphia: J. B. Lippincott.

Novacheck, T. (1998). The biomechanics of running. Gait and Posture 7, 77-95.Paul, G. S. (1998). Limb design, function and running performance in ostrich-mimics

and tyrannosaurs. Gaia 15, 257-270.Paul, G. S. and Christiansen, P. (2000). Forelimb posture in neoceratopsian

dinosaurs: implications for gait and locomotion. Paleobiology 26, 450-465.Pennycuick, C. J. (1975). On the running of the gnu (Connochaetes taurinus) and

other animals. J. Exp. Biol. 63, 775-799.Pezzack, J. C., Norman, R. W. and Winter, D. A. (1977). An assessment of

derivative determining techniques used for motion analysis. J. Biomech. 10, 377-382.Pike, A. V. L. and Alexander, R. McN. (2002). The relationship between limb-

segment proportions and joint kinematics for the hind limbs of quadrupedalmammals. J. Zool. 258, 427-433.

Reinschmidt, C., van den Bogert, A. J., Lundberg, A., Nigg, B. M., Murphy, N.,Stacoff, A. and Stano, A. (1997). Tibiofemoral and tibiocalcaneal motion duringwalking: external vs. skeletal markers. Gait Posture 6, 98-109.

Ren, L. and Hutchinson, J. R. (2008). The three-dimensional locomotor dynamics ofAfrican (Loxodonta africana) and Asian (Elephas maximus) elephants reveal asmooth gait transition at moderate speed. J. R. Soc. Interface 5, 195-211.

Ren, L., Jones, R. K. and Howard, D. (In press). Whole body inverse dynamics overa complete gait cycle based only on measured kinematics. J. Biomech.

Roth, V. L. (1992). Inferences from allometry and fossils: dwarfing of elephants onislands. Oxf. Surv. Evol. Biol. 8, 259-288

Rubenson, J., Lloyd, D. G., Besier, T. F., Heliams, D. B. and Fournier, P. A.(2007). Running in ostriches (Struthio camelus): three-dimensional joint axesalignment and joint kinematics. J. Exp. Biol. 210, 2548-2562.

Schwerda, D. (2003). Analyse Kinematischer Parameter der Lokomotion vonLoxodonta africana (Proboscidea: Elephantidae). Diplomarbeit, Friedrich-Schiller-Universität Jena, Germany.

Seyfarth, A., Geyer, H. and Herr, H. (2003). Swing-leg retraction: a simple controlmodel for stable running. J. Exp. Biol. 206, 2547-2555.

Shakespeare, W. (1609). The History of Troilus and Cressida.Shoshani, J. (1992). Elephants: Majestic Creatures of the Wild. New York: Rodale

Press.Smuts, M. M. S. and Bezuidenhout, A. J. (1993). Osteology of the pelvic limb of the

African elephant (Loxodonta africana). Onderstepoort J. Vet. Res. 60, 1-14.Smuts, M. M. S. and Bezuidenhout, A. J. (1994). Osteology of the pelvic limb of the

African elephant (Loxodonta africana). Onderstepoort J. Vet. Res. 61, 51-66.Tennent, J. E. (1999). Sketches of the Natural History of Ceylon. New Delhi: Asian

Educational Services.van Weeren, P. R., van den Bogert, A. J. and Barneveld, A. (1988). Quantification

of skin displacement near the carpal, tarsal and fetlock joints of the walking horse.Equine Vet. J. 20, 203-208.

van Weeren, P. R., van den Bogert, A. J. and Barneveld, A. (1990). A quantitativeanalysis of skin displacement in the proximal parts of the limbs of the walking horse.Equine Vet. J. Suppl. 9, 110-119.

Weissengruber, G. E., Fuss, F. K., Egger, G., Stanek, G., Hittmair, K. M. andForstenpointner, G. (2006). The elephant knee joint: morphological andbiomechanical considerations. J. Anat. 208, 59-72.

Winter, D. A., Sidwall, H. G. and Hobson, D. A. (1974). Measurement and reductionof noise in kinematics of locomotion. J. Biomech. 7, 157-159.

Wood, G. L. (1972). Animal Facts and Feats. New York: Doubleday.


erratum the movements of limb segments and joints...

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