Bipedal versus Quadrupedal Hind Limb and Foot Kinematics in a Captive Sample of Papio anubis: Setup and Preliminary Results

Bipedal versus Quadrupedal Hind Limband Foot Kinematics in a Captive Sampleof Papio anubis: Setup and Preliminary Results

Gilles Berillon & Guillaume Daver &

Kristiaan D’Août & Guillaume Nicolas &

Bénédicte de la Villetanet & Franck Multon &

Georges Digrandi & Guy Dubreuil

Received: 20 February 2009 /Accepted: 16 October 2009 /Published online: 1 April 2010# Springer Science+Business Media, LLC 2010

Abstract Setups that integrate both kinematics and morpho-functional investigationsof a single sample constitute recent developments in the study of nonhuman primatebipedalisms. We introduce the integrated setup built at the Primatology Station of theFrench National Centre for Scientific Research (CNRS), which allows analysis of bothbipedal and quadrupedal locomotion in a population of 55–60 captive olive baboons. Asa first comparison, we present the hind limb kinematics of both locomotor modalities in10 individuals, focusing on the stance phase. The main results are: 1) differences inbipedal and quadrupedal kinematics at the hip, knee, and foot levels; 2) a variety of footcontacts to the ground, mainly of semiplantigrade type, but also of plantigrade type; 3)equal variations between bipedal and quadrupedal foot angles; 4) the kinematics of the

Int J Primatol (2010) 31:159–180DOI 10.1007/s10764-010-9398-2

G. Berillon (*)UPR 2147 CNRS, Dynamique de l’Évolution Humaine, 75014 Paris, Francee-mail: [email protected]

G. DaverDépartement de Préhistoire, Musée de l’Homme, Muséum National d’Histoire Naturelle, 75116 Paris,France

K. D’AoûtFunctional Morphology, Department of Biology, University of Antwerp, Antwerp, Belgium

K. D’AoûtCentre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium

G. Nicolas : F. MultonLaboratoire M2S Mouvement, Sport, Santé (Physiologie et Biomécanique) UFR-APS,Université Rennes 2 – ENS Cachan, Rennes, France

B. de la VilletanetLAPP, UMR 5199 PACEA, Université Bordeaux 1, Bordeaux, France

G. Digrandi :G. DubreuilStation de primatologie, CNRS, Rousset sur Arc, France

foot joints act in coordinated and stereotyped manners, but are triggered differentlyaccording to whether the support is bipedal or quadrupedal. Although very occasionallyrealized, the bipedal walk of olive baboon appears to be a habitual and nonerraticlocomotor modality.

Keywords bipedalism . foot stance . hind limb . integrated setup . kinematics .

olive baboon . quadrupedalism

Introduction

Kinematics and the functional morphology of nonhuman primates are 2 researchfields that provide crucial information that can be used to evaluate early hominidlocomotor modes (Coppens and Senut 1991; Crompton and Günther 2004; Franzenet al. 2003; Ishida et al. 2006; Kimura et al. 1996; Meldrum and Hilton 2004;Preuschoft 1970, 1971, 1973; Strasser et al. 1998; this issue). Kinematicinvestigations regard primates mainly as completely integrated systems anddocument movements quantitatively. Functional morphological analyses often startfrom anatomical descriptions —usually no more than 1 or 2 traits— and aim to relatethese to function. For technical reasons, these 2 complementary research fields areusually undertaken separately. Doing so has produced a great deal of valuable data,but correlations among form, function, and locomotor output often remainhypothetical. Because kinematic and kinetic data are still relatively scarce, it isoften difficult to evaluate functional hypotheses deduced from morpho-functionalanalyses, usually performed on cadavers, in light of in vivo experimental (motion)data. From a paleoanthropological perspective, Susman and Stern (1991, p. 126)have stated that “until we can understand the relationships between structure andfunction in living models, we will never be able to place any confidence in ourinferences about fossil forms that are represented by fragmentary and incompleteremains.” This holds true also when studying bipedal locomotion, a hot topic inpaleoanthropological discussions. Therefore collection of data on both movementsand anatomy will improve our understanding of the process of acquisition ofbipedality in human evolution.

Integrated studies of nonhuman primate bipedalism have been developed sincethe late 1990s (Aerts et al. 2000; D’Août et al. 2001, 2002; Hirasaki et al. 2004;Nakatsukasa et al. 1995, 2004, 2006; Ogihara et al. 2007; Vereecke and Aerts 2008;Vereecke et al. 2003, 2004, 2005, 2006a, b) and are based on pioneering earlierresearch (Crompton et al. 1996; Elftman 1944; Jenkins 1972; Ishida et al. 1974;Kimura 1985, 1990; Kimura et al. 1979; Li et al., 1996; Okada 1985; Tardieu et al.1993; Yamazaki et al. 1979). For historical reasons and because of the typicallylimited access to primates, these integrated studies have been developed for only afew species, e.g., Hylobates lar, Macaca fuscata, Pan paniscus. In addition, theytypically use few individuals and focus on cross-sectional analyses. Despite theirlimitations, these integrated studies have provided a large amount of original dataand have put human and nonhuman bipedalism into a comparative perspective. Thiscan be illustrated by studies of the transverse midtarsal joint in nonhuman primates.In humans, the stability of the transverse midtarsal joint has been associated with an

160 G. Berillon et al.

efficient support for bipedal locomotion, whereas the compliant nonhuman primatefoot with a midtarsal break has been associated with inefficient bipedalism (Bojsen-Moller 1979; Elftman and Manter, 1935a, b; Lewis 1989). As a consequence, it isimplicit in the paleoanthroplogical literature that a hominid with some degree ofcompliancy in the midfoot should not be considered an efficient biped (see Ward2002 for a complete review of the literature). Researchers have challenged theanatomical basis of midfoot flexibility in some nonhuman primates (DeSilva 2010;Günther 1989; Vereecke et al. 2003), and thanks to an integrated analysis, Vereeckeand Aerts (2008) have demonstrated that foot compliance might in fact contributeto a form of propulsion generation in bipedalism in gibbons. This example showshow the analysis of nonhuman-like bipedalism in primates can trigger novelinterpretations of functional anatomy and, as a consequence, provide potentialnew perspectives on bipedalism in early hominids.

Our team is currently developing an integrated technical platform that couplesmotion and anatomical analyses of nonhuman primates at the Primatology Station ofthe French National Centre for Scientific Research (CNRS). We are analyzing boththe kinematics and the anatomy of bipedal vs. quadrupedal locomotion in baboons.We chose baboons because it has been known since the 1970s that they occasionallybut spontaneously walk bipedally in the wild (Hunt 1989; Rose 1976, 1977;Wrangham 1980) as well as in captivity (G. Berillon, pers. obs.). However, thekinematics and kinetics of their bipedal and quadrupedal locomotor behavior are stillpoorly documented (Ishida et al. 1974; Okada 1985; Shapiro and Raichlen 2005), asis their type of foot contact to the ground (Meldrum 1991; Schmitt and Larson1995). We aim at filling this gap and have started by describing bipedal kinematicsof the main segments of the body (Berillon et al. 2010) and describing an integratedsetup for 3D motion capture and anatomical description. In addition, we present theresults of the first comparative analysis of bipedal vs. quadrupedal walking in olivebaboons of a wide age range, focusing on the sagittal kinematics of the hind limband the foot.

Materials and Methods

General Setup

The CNRS Primatology Station in Rousset-sur-Arc (France) houses and breeds baboonsfor scientific investigations. All individuals receive veterinary monitoring from birth onand undergo annual health checks. This baboon population therefore offers anexceptionally valuable basis for joint and long-term motion analysis and anatomicalinvestigations on nonhuman primates. The baboons at the Primatology Station aremainly housed in groups of several tens of individuals. The groups live in open-airenclosures of which the surface areas span between approximately 150 and 500 m², andwhich are connected to permanent shelters by corridors. We selected the group living inenclosure B2F for our studies because 1) the number of baboons is controlled andmaintained at ca. 60 individuals, representing all age classes from newborns (5–6births per year) to old adults (≤18 years old); 2) many individuals spontaneously walkbipedally; 3) the arrangement of the enclosure and its surface area (ca. 300 m²) are

Bipedalism vs. Quadrupedalism in Olive Baboons 161

well-suited to the installation of an open-air motion analysis setup within the enclosureand its immediate periphery; and 4) the proximity of the veterinary building, includinga pharmacy, a laboratory, and the X-ray machine (Mobil X ray generator SAXOAPELEM), allows on-the-spot morphological investigations and thus limits stresswhen capturing the individuals. The connection between the enclosure and the indoorstructure is controlled by several trapdoors, allowing us to adapt the composition ofthe sample in the enclosure for 2–3 h for specific experiments. Each individual isidentified by a numbered collar that is readable on the video footage.

We collect data in 2 ways. First, we have constructed a technical platform toanalyze locomotion in olive baboons within their living environment and throughoutontogeny. It consists of a motion analysis system with high-speed video, force plates,and pressure plates. The motion capture and analysis setup allows for high-frequencyrecordings of baboon locomotion along a horizontal surface and was adapted fromexisting setups (Aerts et al. 2000; D’Août et al. 2001, 2004; Hirasaki et al. 2004;Nicolas et al. 2007; Vereecke et al. 2006a, b). Second, we conduct noninvasivemorphological investigations (weighing, external measurements, radiography) of allindividuals of the population.

We make morphological investigations on anesthetized individuals duringscheduled captures. These consist of external measurements, measurements of jointmobility, weighing, and osteoarticular observations based on X-ray imaging.Captures are conducted every 3 mo under veterinary control, and are the only formof physical interaction allowed with the baboons in the enclosure. We capture thebaboons individually using a restraining nest box. We then transfer the capturedindividual to a cage to receive general anesthesia via intramuscular injection ofImalgène (10–15 mg/kg). Anesthesia lasts ≤30 min, the time required to make theexternal measurements and radiographs, to develop the films, and to weigh theindividuals. We perform additional anatomical investigations —dissections, inertialproperties, 3D imaging, etc.— on cadavers when available.

In conclusion, our research facilities enable us to monitor quantitatively themorphological, functional, and behavioral development, i.e., in a longitudinal studyapproach of each individual in the enclosure with limited stress for the subjects. Ourexperiments have been approved by the Regional Ethics Committee for animalexperimentation of the Midi-Pyrénées Region (Letter MP/01/15/02/08, datedFebruary 20, 2008).

Materials

To date, we have recorded 320 quadrupedal gait sequences. These were performedby all of the individuals >6 mo old, sometimes several times and in some cases atseveral stages of ontogeny. In addition, we recorded 90 bipedal gait sequencesperformed by young individuals (6 mo–6 yr old) in several stages of ontogeny. Forthis initial comparison of bipedal and quadrupedal kinematics, we selected 10 Papioanubis for which we recorded both bipedal and quadrupedal locomotion atequivalent stages in their development, which allows us to limit the effect ofindividual variation when comparing the characteristics of bipedal and quadrupedalgaits. We give general information on these 10 individuals in Table I; ages rangedfrom 0.55 to 5.39 yr and masses from 2.7 kg to 15.2 kg.


Methods

The Motion Capture Setup The motion capture setup is based on a multicamerahigh-speed video recording system. The recording zone is in the southeastern part ofthe open-air enclosure B2F (Fig. 1). To guide the baboons along a regular path, webuilt an elevated, horizontal walkway around which we set up the video cameras.The walkway (podium) is a concrete structure, 80 cm wide, 30 cm high, and 5 mlong, with ramps at each end to maintain continuity with the ground in the enclosure.The walkway runs east to west, parallel to and 3 m away from the southern edge ofthe enclosure. Two free spaces are supplied for force plates and pressure pads(FootScan).

We mounted 4 high-speed digital video cameras (Basler 602fc) outside the fenceon tripods and swivel arms. We equipped each camera with a C-Mount manual lens(8–48 mm F/1.0). We use the three cameras located in the southern part of theobservation area for 3D motion capture within a 2 m-wide field: 1 camera ishorizontally oriented, perpendicular to the long axis of the walkway, at a distance of3.5 m from the center of the recording field and at a height of 40 cm above the top ofthe walkway; 2 cameras are obliquely oriented on either side of the previous camera,ca. 2.5 m away from it, at a height of 1.40 m above the top of the walkway and4.5 m distant from the centre of the recording field. The fourth camera is placedopposite to the first camera, perpendicular to the long axis of the walkway, at a

Table I Composition of bipedal (2P) and quadrupedal (4P) samples used in the study

Name Identification tag Code Sex Gait Age (yr) Mass (kg)

Chris 854 V792BA M 2P 0.67 2.9

4P 0.55 2.7

Chantal 139 V908I F 2P 1.09 4.1

4P 1.09 4.1

Babar 632 V916F M 2P 1.58 5.4

4P 1.88 6.1

Alf 643 V894G M 2P 2.38 7.1

4P 2.39 7.1

Vinci 568 V896F M 2P 3.14 8.3

4P 3.27 8.5

Voltarelle 604 V915F F 2P 3.28 7.3

4P 3.12 7.1

Vernie 638 V903D F 2P 3.28 6.3

4P 3.15 6.1

Victoire 406 V896E F 2P 3.82 10.3

4P 3.63 9.9

Volga 411 V916D F 2P 3.95 12.5

4P 4.09 12.5

Tassadite 606 V893E F 2P 5.39 15.2

4P 5.09 14.5


distance of 9 m from the center of the recording field and covers a 4 m-wide field ofview. We use this camera to record longer sequences —walking, running, transitions,jumping, etc.— and to make a posteriori measurements of speed variations overseveral strides.

Each camera is connected to a workstation by means of 10-m long firewire cablesand an acquisition chart. The workstation is a purpose-built Streamstation. Wecontrol the digital settings of the cameras, their synchronization, and the videorecording periods with Streampix 4.13.1 (Norpix). Synchronous recording by the 4cameras is triggered by a single manual signal. We record four 5-s sequences, i.e.,the maximum duration, simultaneously to the workstation’s random access memory.Next, we select the exploitable portion of the recorded locomotion after visualizationand store it as 4 separate sequences of equal sizes on the hard drive in the originaluncompressed software format (.seq). We then convert these sequences to AVI filesusing motion analysis software, thanks to an automatic exportation procedure inStreampix.

Fig. 1 Plans of the motion capture system as installed in enclosure B2F (a) and of the motion capture area(b). DVC = digital video camera; FP = force plate; FSc = foot scan.


The Streamstation is set up in a wooden shelter built in line with the walkwayfrom which the movements of the baboons can be observed easily. We attract thebaboons to the platform by means of a 0.5-m² mirror positioned at its eastern end,outside the enclosure. We record different modes of locomotion, including walking,running and transitions. For this study we selected video sequences containing at ≥2complete walking cycles performed at constant speed at the subject’s own pace; weselected bipedal gaits when the baboon’s hands were hanging free and it was notcarrying a load.

Owing to the baboon’s activity rhythm and the local climate, we made videorecordings from spring to autumn, preferably in the mornings. The winter break isrelatively short and does not cause significant gaps in the longitudinal monitoring ofimmature individuals.

We made video recordings at a frame rate of ≥100 fps and a resolution of 656×490 pixels. We kept exposure as short as possible, with a shutter ideally <250,depending on the available natural light.

The Multisegment Model On each video frame, we digitized 19 anatomical referencepoints, of which we used 9 to construct a 6-linked segment model to analyze thekinematics of the hind limb in a sagittal plane (Fig. 2a). We performed the entireprocedure of digitizing reference points and calculating motion parameters with

Fig. 2 The anatomical landmarks and their osteological correspondence as seen in lateral view on x-rayimaging of individual 854 in a resting position (a) and the sagittal joint angles as calculated from theseanatomical landmarks (b).


Kwon3D software (Visol). The 9 reference points are as follows: sagittally anddorsally, the points corresponding to the base of the neck and the base of tail, andthen on the right side, the greater trochanter, the most anterior point of the patella,the assumed axis of the ankle joint and most posterior point of the heel, 2 plantarpoints corresponding to the cuboid and the lateral metatarsophalangeal joint, and thetip of the third toe.

Because the midfoot of a baboon is not rigid during the stance phase (Okada1985; Meldrum 1991; Schmitt and Larson 1995), it was necessary to measure, as faras technically feasible, the relative movements of the proximal tarsus on the lowerleg (taking place in the talocrural joint, essentially), and of the midfoot (the distaltarsus and the metatarsus) against the proximal tarsus. This proved possible byidentifying ≥1 anatomical point between the talocrural joint and the metatarsopha-langeal joint; both are classic reference points in the literature. Vereecke and Aerts(2008) recently applied this principle to the highly compliant gibbon’s foot; theyused the tarsometatarsal joint on the assumption that motion essentially takes placeat this level, as proposed by recent experimental analysis (DeSilva 2010; Hirasakiand Kumakura 2003); sagittal motion at the midtarsal joint level has already beendemonstrated for other locomotor modes such as leaping (Günther 1989). Our ownradiological observations and manipulations of cadavers and anesthetized individualsconfirm that foot compliancy occurs in the tarsometatarsal and transverse midtarsaljoints. For the moment, however, it is impossible to assess the relative importance ofthe mobility of each joint, and to discern the exact position of these 2 joints in thevideo recording. Therefore, as a first approximation, we selected the point located onthe plantar face of the foot corresponding to the intersection of the axis of theproximal foot —represented by the plantar face of the heel— with the midfoot axisrepresented by the plantar face of the metatarsus. We digitized this point directly inthe frames, where it appears to be located just behind the tuberosity of the fifthmetatarsal bone.

We transformed the 20 original sets of 2D coordinates into 20 calibrated sets ofcoordinates, i.e., coordinates that are explained in a single common reference frame,in this case based the walkway, for each sequence with the KwonCC calibrationprocedure. This involves digitizing reference points located on a calibration frame(1 m long, 1 m high, and 0.7 m wide) that was placed in the video recording field atthe beginning of each recording session. The DLT calibration procedure in theKwonCC module produced an average reconstruction error of 0.79 mm.

Spatiotemporal Parameters and Joint Angles From the calibrated reference pointcoordinates, we calculated absolute and dimensionless spatiotemporal parameters aswell as the joint angles of the lower limb following the procedure described inBerillon et al. (2010). We computed the spatiotemporal parameters absolute stridelength (m), stride duration (s), stride frequency (s–1; we define a stride as onecomplete gait cycle from touchdown of a foot to the next touchdown of the samefoot) and speed (m s–1), the duty factor, and dimensionless speed. We incorporatedavailable spatiotemporal parameters and values for hip and knee angles associatedwith the bipedal gait (Berillon et al. 2010) into the full data set, includingquadrupedal spatiotemporal parameters, quadrupedal hip and knee joint kinematics,and quadrupedal and bipedal joint kinematics of the foot. With regard to the foot


angles, in addition to the classical ankle joint angle, we computed the talocrural jointangle, the metatarsophalangeal joint angles, and the midfoot angle (Fig. 2b). We firstpresent charts of the average movement over time, expressed as a fraction of cycleduration, of the bipedal and quadrupedal hip, knee, and ankle joints and theirvariation at key events in the complete cycle: maximum and minimum, localmaximum and minimum, at right and left foot contacts and at right and left toe-off.For the stance phase of the foot, we present the average and individual movementsof the foot joints over time, expressed as a fraction of the stance phase duration. Wetested differences between bipedal and quadrupedal joint angles at gait events usinga covariance analysis procedure (ANCOVA, Statistica 6.0), with the joint angles asdependent variable, the gait as independent variable, and the dimensionless speed ascovariate.

Results

Spatiotemporal Parameters

Table II shows individual and average values, SD, and the range of calculatedspatiotemporal parameters. During quadrupedal walking, the stance phase isrelatively short compared to bipedal walking, representing 66.4±0.3% of the cycleduration (vs. 69.9±0.3% when the gait is bipedal); the stride length and strideduration are much greater (0.67±0.15 m vs. 0.52±0.03 m, and 1.05±0.05 s vs. 0.69±0.16 s) and the absolute speed is lower (0.64±0.15 ms–1 vs. 0.79±0.19 ms–1).

Joint Angles of the Lower During a Stride

Table III and Fig. 3 summarize the changes of average hip, knee, and ankle anglesand their variations during bipedal and quadrupedal locomotion over timeexpressed as a fraction of a cycle. Generally speaking, bipedal movements aremore variable than quadrupedal ones, in terms of values as well as the timing ofoccurrences.

Considering the joints successively, we observed that the hip is always bent, butsignificantly less so at any time in the bipedal than the quadrupedal cycle (Table IV).This is related to the position of the trunk, which is tilted sharply forward duringquadrupedal locomotion. The peak of flexion is reached at ca. 58% of the cycle inboth modes, before the toe-off and shortly after contact of the opposite foot. Thetotal range of motion during a quadrupedal cycle (52.8°±4.8) is larger than during abipedal cycle (34°±7.1).

The knee is also always bent in the quadrupedal gait cycle, but significantly lessthan in the bipedal gait. Minimum flexion is reached at initial foot contact and thepeak of flexion occurs at ca. 75% of the cycle in both modes, well after toe-off in thequadrupedal gait cycle. The range of knee flexion is large but significantly smallerduring quadrupedal locomotion than in bipedal locomotion (50.5°±6 vs. 65.1°±8.3).In quadrupedal locomotion, knee flexion increases in 2 phases: 1) from the initialfoot contact to the contralateral toe-off and 2) from the contralateral foot-contact toits maximum, after toe-off; between both phases, knee flexion varies very little. In


bipedal locomotion, the knee flexion gradually increases from the initial foot contactto its maximum. Finally, in both the bipedal and quadrupedal gait cycles, there is lessvariation in the knee angle than in those observed for the hip and the ankle.

With regard to the ankle joint, angles in bipedal and quadrupedal gaits followsimilar profiles and their values differ only slightly; in quadrupedal locomotion, thevalues are significantly lower around the foot contact. Two main phases of extensionand flexion are separated by a peak of minimum flexion at toe-off. There isremarkable variation in the time of the first peak of flexion, both in bipedal and inquadrupedal gaits.

The Foot During the Stance Phase

We paid special attention to the foot during stance phase in both bipedal andquadrupedal locomotions.

Table II Individual and average (mean±SD) lower leg length and spatiotemporal parameters

Individual(medal)

Lower leglength (m)

Gait(2P/4P)

Stridelength(m)

Strideduration(s)

Stridefrequency(1/s)

Absolutespeed (m/s)

Dimensionless speed

Dutyfactor

854 0.12 2P 0.52 0.51 1.96 1.02 0.94 0.67

4P 0.42 1.04 0.96 0.40 0.41 0.67

139 0.13 2P 0.45 0.76 1.32 0.60 0.52 0.72

4P 0.49 1.04 0.96 0.47 0.41 0.69

632 0.14 2P 0.56 0.60 1.67 0.94 0.82 0.73

4P 0.64 0.98 1.02 0.65 0.56 0.64

643 0.15 2P 0.50 0.83 1.20 0.60 0.49 0.73

4P 0.65 1.17 0.85 0.56 0.43 0.71

568 0.17 2P 0.54 0.53 1.89 1.02 0.79 0.68

4P 0.65 1 1.00 0.65 0.49 0.65

604 0.15 2P 0.50 0.58 1.72 0.87 0.72 0.64

4P 0.63 1.03 0.97 0.61 0.50 0.67

638 0.16 2P 0.50 0.61 1.64 0.83 0.66 0.67

4P 0.67 1.03 0.97 0.65 0.52 0.65

406 0.20a 2P 0.56 0.68 1.47 0.83 0.60 0.68

4P 0.83 1.06 0.94 0.78 0.62 0.62

411 0.19a 2P 0.55 0.74 1.35 0.75 0.55 0.73

4P 0.82 1.09 0.92 0.75 0.60 0.63

606 0.20a 2P 0.50 1.05 0.95 0.47 0.34 0.72

4P 0.93 1.04 0.96 0.89 0.62 0.66

Mean±SD 0.16±0.03 2P 0.52 ±0.03

0.69±0.16

1.52 ±0.32

0.79±0.19

0.64±0.18

0.699±0.3

4P 0.67±0.15

1.05±0.05

0.96±0.05

0.64±0.15

0.52 ±0.08

0.664±0.3

a Calculated from video recordings.


Tab

leIII

Tim

eof

occurrence

ofcharacteristic

eventsof

thestride

(expressed

asafractio

nof

cycleduratio

n)andaverageangles

atcharacteristic

events(m

ean±SD)

Gait

Initial

foot

contact

Opp

osite

toeoff

Minim

umankleangle

Opp

osite

foot

strike

Maxim

umhipangle

ToeOff

Maxim

umankleangle

Minim

umkn

eeangle

Finalm

inim

umankleangle

Final

foot

contact

Range

ofmotion

Tim

eof

occurrence

2P0±0

19.4±6.5

34.6±10

.051

.2±2.6

57.9±3.2

69.9±3.4

67.5±4.2

74.7±3.1

84.3±3.4

100±0

4P0±0

16.4±2.6

31.2±8.8

50.8±2.3

58.6±2.6

66.4±2.3

65.6±2.6

76.5±2.0

83.1±3.2

100±0

Hip

angle

2P10

4.8±9.8

110.2±8.3

131.8±8.1

134.6±9.4

124.5±11.5

105.9±10

.834

.0±7.1

4P59

.1±4.0

65.9±4.2

105.0±5.6

110.9±5.0

103.8±4.6

62.4±6.2

52.8±4.8

Kneeangle

2P12

4.8±6.6

102.9±5.8

85.5±6.1

66.8±9.0

63.7±8.8

127.1±8.4

65.1±8.3

4P13

4.5±3.9

117.7±2.9

116.6±5.8

102.4±4.3

86.9±6.4

137.1±5.5

50.5±6.0

Ank

leangle

2P119.6±8.0

98.8±9.5

89.5±11.7

100.0±13.6

122.1±12

.112

4.1±13

.010

0.8±7.6

122.0±8.7

42.1±7.6

4P112.4±9.1

90.5±6.2

84.3±7.8

93.5±9.2

118.7±6.5

119.6±7.1

90.1±7.3

115.2±5.5

37.9±9.3

Talocrural

angle

2P124.4±6.4

109.9±6.8

103.3±8.4

105.0±8.0

117.0±10.5

119.9±11.0

103.6±6.7

125.0±6.0

30.5±6.8

4P114.2±4.8

95.9±8.7

97.1±7.3

99.5±7.2

118.2±6.3

119.6±7.4

95.1±5.6

114.7±4.8

29.6±7.5

Midfoot

angle

2P14

9.0±3.6

136.2±8.2

128.8±6.6

137.5±7.8

156.7±7.7

156.6±8.1

144.4±4.2

148.3±4.7

32.4±7.7

4P15

4.4±5.4

148.9±9.1

132.9±7.8

137.0±5.5

149.5±7.4

149.5±7.1

145.5±6.8

152.4±5.8

30.5±7.1

Metatarsophalangeal

angle

2P16

5.1±5.9

178.3±5.6

173.5±5.7

144.9±14.1

153.5±12

.913

7.3±10

.517

9.4±27

.416

4.8±6.9

71.5±40

.1

4P16

4.0±6.9

178.0±5.1

176.5±6.2

150.8±11.4

150.5±7.7

146.7±10

.116

2.2±4.8

164.2±6.0

48.2±11.1


Type of Foot Contact with the Ground In most cases the foot touches the ground ina rather horizontal position in both bipedal and quadrupedal gaits. It is placedforward, in front of the hip; the knee and the ankle joint appear to be at theirmaximum extension and plantarflexion respectively. We observed 3 main patternsof foot contact with the ground (Fig. 4): 1) The foot comes into contact with theground at its middle part, from the distal tarsus to the metatarsophalangeal joint.Toe contact occurs later, while the heel is raised and never touches the ground.During quadrupedal locomotion, a slight and temporary drop of the proximal footis almost systematically observed immediately after the initial contact, but the heelnever touches the ground. This is the most frequent pattern in both gaits (7/10quadrupedal and 8/10 bipedal). 2) The foot contact is initiated simultaneously bythe plantar surfaces of the midfoot and the toes; we observed this in the 2 youngestsubjects of the sample during bipedal locomotion (Ind. 854 and Ind. 139), and in 1individual during quadrupedal locomotion (Ind. 638). 3) The foot contact issimultaneously initiated by the plantar face of the heel and the midfoot and

Fig. 3 Comparison of mean changes of the hind limb angles and the events through a bipedal and aquadrupedal stride. IFC = initial foot contact; OTO = opposite toe off; OFC = opposite foot contact;TO = toe off; FFC = final foot contact). Open symbols = bipedal walking; solid symbols = quadrupedalwalking.


Tab

leIV

pvalues

forANCOVA

analyses

Initial

foot

contact

Opp

osite

toeoff

Minim

umankleangle

Opp

osite

foot

strike

Maxim

umhipangle

Toeoff

Maxim

umankleangle

Minim

umkn

eeangle

Final

minim

umankleangle

Final

foot

contact

Hip

angle

0.00

160

00

00

00

00.038

Kneeangle

00

00

00

00

00

Ank

leangle

0.16

70.009

0.074

0.26

80.73

20.255

0.187

00.074

0.031

Talocrural

angle

0.00

440.002

0.047

0.12

60.46

10.92

0.591

0.02

40.047

0.001

Midfoot

angle

0.03

70.014

0.321

0.78

90.78

0.043

0.046

00.321

0.258

Metatarsophalangeal

angle

0.89

0.327

0.067

0.57

40.58

80.305

0.079

0.10

70.067

0.491


continues by the entire sole of the foot; this describes a plantigrade stance phasewith no heel-strike. Very soon after the initial contact, the proximal foot movesupward. We observed this in 2 quadrupedal sequences (Ind. 411 and Ind. 568,respectively, a 4-yr-old female and a 3-yr-old male), but not in any instance ofbipedal locomotion.

To summarize, during both bipedal and quadrupedal locomotion in olive baboons,the foot usually contacts the ground in a semiplantigrade manner. Nevertheless,variants exist up to plantigrade support in quadrupedal locomotion, which has notbeen described in the literature.

Pedal Joint Angles During the Stance Phase Table III and Fig. 5 show the changesof average foot angles and their variations for bipedal and quadrupedal walking overtime expressed as a fraction of stance phase duration. Variation in the bipedal andquadrupedal angles at each event is similar, in contrast to what is observed for theankle angle. The talocrural angle in both bipedal and quadrupedal gaits is >90°during the stance phase, which means that the talocrural joint is kept slightlyextended; talocrural extension is at its maximum at the beginning and end of the

Fig. 4 Lateral views of the 3 observed modalities of foot contact to the ground.


stance phase and reaches its minimum around midstance. The extension of thetalocrural joint is more pronounced in bipedal than quadrupedal mode, andsignificantly so during the first half of the stance phase (Table IV). The midfoot isbent dorsally concave, with flexion at its maximum at approximately midstance.This flexion is significantly higher in a bipedal gait cycle at the beginning of thestance phase. This tendency is then progressively reversed, with the midfootsignificantly more bent during the quadrupedal gait at toe-off. Thus, at the beginningof the stance phase of a bipedal gait cycle, the proximal foot is raised in a relativelymore elevated position than in quadrupedal locomotion. We observed no significantdifference between the bipedal and the quadrupedal profiles of the metatarsopha-langeal joints. After a short period of dorsiflexion at the initial contact, this jointquickly reaches its neutral 180° position. On average, during the second half of thestance phase, the joint dorsiflexes up to a peak at the end of the stance phase, withdorsiflexion then decreasing at toe-off. These average profiles illustrate a general

Fig. 5 Comparison of mean changes of the foot angles and the events through a bipedal and aquadrupedal stance phase. IFC=initial foot contact; OTO=opposite toe off; MAA=maximum ankle angle;OFC=opposite foot contact; TO=toe off. Open symbols=bipedal walking; solid symbols=quadrupedalwalking.


increase in the dorsiflexion of the tarsometatarsal complex during the first half of thestance phase; this movement is then reversed while the metatarsophalangeal jointsstarts dorsiflexing.

To understand the variation observed, we now focus on the way the joints ofthe individual study subjects behave (Fig. 6). In general, for each type oflocomotion, we observed that individual movements follow a rather similar patternbut the relative duration of the different periods varied widely among the individualsin the sample. The foot kinematics during the bipedal stance phase can be describedas follows:

& The touchdown period: The metatarsophalangeal dorsiflexion quickly returnsfrom a dorsiflexed posture to reach full extension at 10–15% of the stance phase,while the talocrural joint and the midfoot gradually dorsiflex.

& The loading period: The dorsiflexion of the talocrural joint and the midfootincreases to maximum flexion at 35–70% of the stance phase depending on

Fig. 6 Individual changes over time of the foot angles through a bipedal (a) and a quadrupedal (b) stancephase.


individuals. No movement occurs at the metatarsophalangeal joint. At the end ofthe loading period, the plantar surface of the proximal tarsus is in an elevatedposition.

& The tarsometatarsal rise period: The metatarsophalangeal joint dorsiflexesleading to a regular lifting of the tarsometatarsal segment; simultaneously, thedorsiflexion of the talocrural joint and the midfoot decreases. The peak ofmaximum metatarsophalangeal dorsiflexion and the peaks of minimum talocruraland midfoot dorsiflexion are reached simultaneously at 85–95% of the stancephase.

& The push-off period: The metatarsophalangeal dorsiflexion quickly decreaseswhile the talocrural joint and the midfoot begin a second period of dorsiflexion.

The foot kinematics during the quadrupedal stance phase can be described as follows:

& The touchdown period: The talocrural joint quickly dorsiflexes while the midfootmoves in the opposite direction; the dorsiflexion of the metatarsophalangeal jointlessens until it is fully extended. This period ends at 10–20% of the stance phase.

& The loading period: no significant motion occurs at the talocrural joint, while themidfoot dorsiflexes. The metatarsophalangeal joint remains in its slightly extendedposition. The peak of maximum midfoot flexion is reached at the moment whenmetatarsophalangeal dorsiflexion begins, at 40–75% of the stance phase.

& The tarsometatarsal rise period: talocrural and midfoot dorsiflexion both lessen,while the metatarsophalangeal joint dorsiflexes simultaneously; these peaks ofminimum (for the talocrural joint and the midfoot) and maximum (for themetatarsophalangeal joint ) dorsiflexion are reached at 85–95% of the stance phase.

& The push-off period: the metatarsophalangeal dorsiflexion quickly lessens whilethe talocrural joint and the midfoot begin a second phase of dorsiflexion.

Individual variation is important, as highlighted by the characteristics of thetouchdown to tarsometatarsal rise periods of individual 139 in quadrupedal locomotion.Although touchdown is immediately followed by a rapid decreasing of themetatarsophalangeal dorsiflexion until it reaches its neutral position, which is observedin all other individuals of our sample, it is as well immediately followed by adorsiflexion of the midfoot. In the other individuals, the dorsiflexion of the midfootremains constant or more often decreases, at this time of the stance phase. In addition,the metatarsophalangeal joint, after reaching its neutral position, immediatelydorsiflexes until it reaches its maximum. This dorsiflexion is usually initiated later inthe other individuals, whereas almost no motion occurs at the talocrural and midfootlevel during that period.

To summarize, the kinematics of the talocrural joint, the midfoot and themetatarsophalangeal joints act in a coordinated manner, but are triggered differentlyaccording to whether the support is bipedal or quadrupedal. In bipedal locomotion,the tarsometatarsal complex dorsiflexes gradually as soon as the foot touches theground, while in quadrupedal locomotion, the stance phase starts with a decreasingof the midfoot dorsiflexion; as a consequence, the posterior foot slightly collapses atthe initiation of the quadrupedal touchdown. We did not observe this difference atthe ankle kinematics level; this could be explained by the method of measuring theankle angle, which combines both talocrural and midfoot kinematics.


Discussion and Conclusion

Baboons are conventionally described as committed quadrupedal primates (Fleagle1988; Rose 1973). They are also known to occasionally and spontaneously walkbipedally (Hunt 1989; Rose 1976, 1977; Wrangham 1980). However, precisekinematics of both locomotor modes remain rare and include few individuals (Ishidaet al. 1974; Okada 1985; Shapiro and Raichlen 2005). As far as lower limb and footkinematics and stance phase descriptions are concerned, a total of 4 individuals havebeen observed (Meldrum 1991; Okada 1985; Schmitt and Larson 1995). We arecurrently documenting movements of unrestricted animals and testing their mobilityin passive manipulation and X-ray imaging. We have provided original data from aninitial sample of 10 Papio anubis, focusing here on lower limb and foot kinematicsin bipedal vs. quadrupedal locomotion. We describe the trunk and hind limb bipedalkinematics elsewhere (Berillon et al. 2010).

As far as the foot stance phase is concerned, Okada (1985) noted that bipedal andquadrupedal locomotor modes were very similar and of semiplantigrade type for 1individual (Papio hamadryas). This type of semiplantigrade foot contact was alsohighlighted for 3 other baboons (1 Papio ursinus and 2 Papio anubis) inquadrupedal locomotion (Meldrum 1991; Schmitt and Larson 1995). Our observa-tions of a larger sample in both bipedal and quadrupedal locomotion demonstrate avariety of foot contacts, from semiplantigrady, which we observed most frequentlyin our sample, to full-fledged plantigrady, observed only in quadrupedallocomotion.

Our qualitative observations are supported by the data concerning foot kinematicsduring the stance phase.The multisegment anatomical model allows a quantitativedecomposition of both bipedal and quadrupedal stance phases at an individual level.This approach is based on observations of midfoot flexibility in many nonhumanprimates, demonstrated early on in the chimpanzee (Elftman and Manter 1935a, b),and later described in a variety of nonhuman primates (D’Août et al. 2002; Gebo1992; Günther 1989; Meldrum 1991; Schmitt and Larson 1995; Vereecke and Aerts2008; Vereecke et al. 2005). Researchers have evaluated this midfoot flexibilityanatomically (Bojsen-Moller 1979; Lewis 1989), although some have challenged itsanatomical origin (Günther 1989; DeSilva 2010). In several analyses of bipedal andquadrupedal hindlimb kinematics of nonhuman primates, researchers have modeledthe foot as a rigid segment, as it is in human (D’Août et al. 2002; Hirasaki et al.2004; Yamazaki et al. 1979). One reason for this methodological choice could relateto the available recording tools: relatively low speed and resolution recording did notprovide frames of sufficient quality that would allow digitization of landmarks otherthan the usual, well-identified ones. In addition, as far as the evolution of the anklejoint angle through a stride is concerned, one can make a direct comparison withhumans. Okada (1985) was the first to propose a quantified kinematic analysis of thecompliant foot, based on the virtual division of the foot into several “blocks”. Thisstudy was very innovative, although its approach might not be trivial to implementin a highly reproducible manner. More recently, Vereecke and Aerts (2008) proposedan approach using high-speed video sequences and their analysis based on theidentification of anatomical referenced points for gibbons (Hylobates lar): theycalculated the position of the tarsometatarsal joint from highly reproducible external


referenced points via a triangulation procedure, assuming that the flexion mainlyoccurs at this level and that it is thus negligible at the midtarsal joint (DeSilva 2010;contra Bojsen-Moller 1979 and Elftman and Manter 1935a, b). In baboons, ourmanipulations of captured and anethesized individuals of the sample and of cadaversshowed that nonnegligible motion occurred at both the transverse midtarsal joint andthe metatarsophalangeal joint level, although it was not possible to measure theirrelative importance at this stage. Unfortunately, we could not identify these 2 jointson the video sequences by proper external reference points. We thus chose to build apoint at the midfoot level that represents the intersection of 2 visible axes, those ofthe proximal foot and of the metatarsus. The angle thus represents the total flexionthat occurs in the joints of the tarsometatarsal complex. Whatever the methodology,use of a multisegment anatomical model of the foot provides innovative results.Vereecke and Aerts (2008) showed that the midfoot dorsiflexes during the stancephase in gibbons and that “this midfoot dosiflexion will stretch the tendons andligaments running across the plantar side of the foot, potentially storing elasticenergy and eventually contributing to propulsion generation at push-off.” In olivebaboons, we show that the dorsiflexion of the midfoot increases from the touch-down phase to the initiation of the metatarsophalangeal dorsiflexion, as in gibbons,favoring the rising of the tarsus while the metatarsus and the toes remain on theground. Could this mechanism potentially contribute to storing elastic energy?Kinetics for baboons must be measured to evaluate this point. Nevertheless, weobserved that this increasing dorsiflexion usually stops earlier than in gibbons (50%and 80%, respectively), and at very variable fractions of the stance phase (from 35%to 70%). This seems to imply a distinctive form of foot mechanics involved duringthe bipedal gait in baboons.

Because baboons are highly adapted quadrupedal primates, one could expect thatquadrupedal kinematics, especially at the foot level, would be less variable thanthose of the less frequently used bipedal locomotor mode. D’Août et al. (2004) usedthis hypothesis to explain the higher variability in bipedal vs. quadrupedal hindlimbkinematics in the bonobo. Although bipedal kinematics of the hip and knee are morevariable than those in the quadrupedal locomotion of olive baboons, our data do notsupport this hypothesis due to the similarity in variation for bipedal and quadrupedalfoot kinematics. Moreover, our analysis of the individual joint angle trajectoriesdemonstrates that joint kinematics are synchronized for both bipedal andquadrupedal locomotion; they follow very similar modalities from one individualto the other but the timing is very variable. Finally, significant differences betweenbipedal and quadrupedal kinematics of the talocrural joint and the midfoot exist. Inparticular, in quadrupedal locomotion the stance phase is initiated by a phase ofdecreasing of the midfoot dorsiflexion. Thus, it seems that motions involved inbipedal and quadrupedal locomotions of olive baboons act in 2 well-coordinated andstereotyped manners.

Terrestrial bipedal walking in baboons must be seen as a proper and not erraticlocomotor mode, even though the species is adapted to another type of locomotion,i.e., terrestrial quadrupedalism. We suggest that the same might hold true for the veryearly hominids, in which terrestrial bipedalism should be seen as a usual locomotormodality, although their anatomy retained several or many traits that would fit betterto arboreal habits (Senut et al. 2001; White et al. 2009).


Acknowledgments We thank the editors of this volume and organizers of the symposium on FunctionalMorphology in Primates in Durham for inviting us to introduce our ongoing program on baboonlocomotion; this contribution is based on this introductory presentation. We also thank the other membersof the Primatology Station, especially Valérie Moulin, for her permanent help. The entire motion capturesystem was set up with the collaboration of P. Trannois (Opto France, France); the Streamstation wasconfigured with the help of T. Lemaire. This research is supported by the Fyssen Foundation (ResearchGrant), and the Groupement de Recherche GDR 2655 of the CNRS (Dir. L. Rosetta). Finally, we thank E.Hirasaki and 2 anonymous reviewers who provided numerous and very constructive comments onprevious versions of the manuscript as well as Joanna M. Setchell, who contributed to the revision of theEnglish and the editing of the final version of the manuscript.

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Documents

Bipedal versus Quadrupedal Hind Limb and Foot Kinematics in a Captive Sample of Papio anubis: Setup and Preliminary Results