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Int J Primatol (2010) 31:159–180
DOI 10.1007/s10764-010-9398-2
Bipedal versus Quadrupedal Hind Limb
and Foot Kinematics in a Captive Sample
of 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 investigations
of a single sample constitute recent developments in the study of nonhuman primate
bipedalisms. We introduce the integrated setup built at the Primatology Station of the
French National Centre for Scientific Research (CNRS), which allows analysis of both
bipedal and quadrupedal locomotion in a population of 55–60 captive olive baboons. As
a first comparison, we present the hind limb kinematics of both locomotor modalities in
10 individuals, focusing on the stance phase. The main results are: 1) differences in
bipedal and quadrupedal kinematics at the hip, knee, and foot levels; 2) a variety of foot
contacts 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
G. Berillon (*)
UPR 2147 CNRS, Dynamique de l’Évolution Humaine, 75014 Paris, France
e-mail: [email protected]
G. Daver
Département de Préhistoire, Musée de l’Homme, Muséum National d’Histoire Naturelle, 75116 Paris,
France
K. D’Août
Functional Morphology, Department of Biology, University of Antwerp, Antwerp, Belgium
K. D’Août
Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium
G. Nicolas : F. Multon
Laboratoire M2S Mouvement, Sport, Santé (Physiologie et Biomécanique) UFR-APS,
Université Rennes 2 – ENS Cachan, Rennes, France
B. de la Villetanet
LAPP, UMR 5199 PACEA, Université Bordeaux 1, Bordeaux, France
G. Digrandi : G. Dubreuil
Station de primatologie, CNRS, Rousset sur Arc, France
160
G. Berillon et al.
foot joints act in coordinated and stereotyped manners, but are triggered differently
according to whether the support is bipedal or quadrupedal. Although very occasionally
realized, the bipedal walk of olive baboon appears to be a habitual and nonerratic
locomotor modality.
Keywords bipedalism . foot stance . hind limb . integrated setup . kinematics .
olive baboon . quadrupedalism
Introduction
Kinematics and the functional morphology of nonhuman primates are 2 research
fields that provide crucial information that can be used to evaluate early hominid
locomotor modes (Coppens and Senut 1991; Crompton and Günther 2004; Franzen
et al. 2003; Ishida et al. 2006; Kimura et al. 1996; Meldrum and Hilton 2004;
Preuschoft 1970, 1971, 1973; Strasser et al. 1998; this issue). Kinematic
investigations regard primates mainly as completely integrated systems and
document movements quantitatively. Functional morphological analyses often start
from anatomical descriptions —usually no more than 1 or 2 traits— and aim to relate
these to function. For technical reasons, these 2 complementary research fields are
usually undertaken separately. Doing so has produced a great deal of valuable data,
but correlations among form, function, and locomotor output often remain
hypothetical. Because kinematic and kinetic data are still relatively scarce, it is
often difficult to evaluate functional hypotheses deduced from morpho-functional
analyses, 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 and
function in living models, we will never be able to place any confidence in our
inferences about fossil forms that are represented by fragmentary and incomplete
remains.” This holds true also when studying bipedal locomotion, a hot topic in
paleoanthropological discussions. Therefore collection of data on both movements
and anatomy will improve our understanding of the process of acquisition of
bipedality in human evolution.
Integrated studies of nonhuman primate bipedalism have been developed since
the 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 earlier
research (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 typically
limited access to primates, these integrated studies have been developed for only a
few species, e.g., Hylobates lar, Macaca fuscata, Pan paniscus. In addition, they
typically use few individuals and focus on cross-sectional analyses. Despite their
limitations, these integrated studies have provided a large amount of original data
and have put human and nonhuman bipedalism into a comparative perspective. This
can 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
Bipedalism vs. Quadrupedalism in Olive Baboons
161
efficient support for bipedal locomotion, whereas the compliant nonhuman primate
foot with a midtarsal break has been associated with inefficient bipedalism (BojsenMoller 1979; Elftman and Manter, 1935a, b; Lewis 1989). As a consequence, it is
implicit in the paleoanthroplogical literature that a hominid with some degree of
compliancy in the midfoot should not be considered an efficient biped (see Ward
2002 for a complete review of the literature). Researchers have challenged the
anatomical basis of midfoot flexibility in some nonhuman primates (DeSilva 2010;
Günther 1989; Vereecke et al. 2003), and thanks to an integrated analysis, Vereecke
and Aerts (2008) have demonstrated that foot compliance might in fact contribute
to a form of propulsion generation in bipedalism in gibbons. This example shows
how the analysis of nonhuman-like bipedalism in primates can trigger novel
interpretations of functional anatomy and, as a consequence, provide potential
new perspectives on bipedalism in early hominids.
Our team is currently developing an integrated technical platform that couples
motion and anatomical analyses of nonhuman primates at the Primatology Station of
the French National Centre for Scientific Research (CNRS). We are analyzing both
the kinematics and the anatomy of bipedal vs. quadrupedal locomotion in baboons.
We chose baboons because it has been known since the 1970s that they occasionally
but spontaneously walk bipedally in the wild (Hunt 1989; Rose 1976, 1977;
Wrangham 1980) as well as in captivity (G. Berillon, pers. obs.). However, the
kinematics and kinetics of their bipedal and quadrupedal locomotor behavior are still
poorly documented (Ishida et al. 1974; Okada 1985; Shapiro and Raichlen 2005), as
is their type of foot contact to the ground (Meldrum 1991; Schmitt and Larson
1995). We aim at filling this gap and have started by describing bipedal kinematics
of the main segments of the body (Berillon et al. 2010) and describing an integrated
setup for 3D motion capture and anatomical description. In addition, we present the
results of the first comparative analysis of bipedal vs. quadrupedal walking in olive
baboons of a wide age range, focusing on the sagittal kinematics of the hind limb
and the foot.
Materials and Methods
General Setup
The CNRS Primatology Station in Rousset-sur-Arc (France) houses and breeds baboons
for scientific investigations. All individuals receive veterinary monitoring from birth on
and undergo annual health checks. This baboon population therefore offers an
exceptionally valuable basis for joint and long-term motion analysis and anatomical
investigations on nonhuman primates. The baboons at the Primatology Station are
mainly housed in groups of several tens of individuals. The groups live in open-air
enclosures of which the surface areas span between approximately 150 and 500 m², and
which are connected to permanent shelters by corridors. We selected the group living in
enclosure B2F for our studies because 1) the number of baboons is controlled and
maintained at ca. 60 individuals, representing all age classes from newborns (5–6
births per year) to old adults (≤18 years old); 2) many individuals spontaneously walk
bipedally; 3) the arrangement of the enclosure and its surface area (ca. 300 m²) are
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G. Berillon et al.
well-suited to the installation of an open-air motion analysis setup within the enclosure
and its immediate periphery; and 4) the proximity of the veterinary building, including
a pharmacy, a laboratory, and the X-ray machine (Mobil X ray generator SAXO
APELEM), allows on-the-spot morphological investigations and thus limits stress
when capturing the individuals. The connection between the enclosure and the indoor
structure is controlled by several trapdoors, allowing us to adapt the composition of
the sample in the enclosure for 2–3 h for specific experiments. Each individual is
identified by a numbered collar that is readable on the video footage.
We collect data in 2 ways. First, we have constructed a technical platform to
analyze locomotion in olive baboons within their living environment and throughout
ontogeny. 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-frequency
recordings of baboon locomotion along a horizontal surface and was adapted from
existing 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 noninvasive
morphological investigations (weighing, external measurements, radiography) of all
individuals of the population.
We make morphological investigations on anesthetized individuals during
scheduled captures. These consist of external measurements, measurements of joint
mobility, weighing, and osteoarticular observations based on X-ray imaging.
Captures are conducted every 3 mo under veterinary control, and are the only form
of physical interaction allowed with the baboons in the enclosure. We capture the
baboons individually using a restraining nest box. We then transfer the captured
individual to a cage to receive general anesthesia via intramuscular injection of
Imalgène (10–15 mg/kg). Anesthesia lasts ≤30 min, the time required to make the
external measurements and radiographs, to develop the films, and to weigh the
individuals. We perform additional anatomical investigations —dissections, inertial
properties, 3D imaging, etc.— on cadavers when available.
In conclusion, our research facilities enable us to monitor quantitatively the
morphological, functional, and behavioral development, i.e., in a longitudinal study
approach of each individual in the enclosure with limited stress for the subjects. Our
experiments have been approved by the Regional Ethics Committee for animal
experimentation of the Midi-Pyrénées Region (Letter MP/01/15/02/08, dated
February 20, 2008).
Materials
To date, we have recorded 320 quadrupedal gait sequences. These were performed
by all of the individuals >6 mo old, sometimes several times and in some cases at
several stages of ontogeny. In addition, we recorded 90 bipedal gait sequences
performed by young individuals (6 mo–6 yr old) in several stages of ontogeny. For
this initial comparison of bipedal and quadrupedal kinematics, we selected 10 Papio
anubis for which we recorded both bipedal and quadrupedal locomotion at
equivalent stages in their development, which allows us to limit the effect of
individual variation when comparing the characteristics of bipedal and quadrupedal
gaits. We give general information on these 10 individuals in Table I; ages ranged
from 0.55 to 5.39 yr and masses from 2.7 kg to 15.2 kg.
Bipedalism vs. Quadrupedalism in Olive Baboons
163
Table I Composition of bipedal (2P) and quadrupedal (4P) samples used in the study
Name
Identification tag
Code
Sex
Chris
854
V792BA
M
Chantal
Babar
Alf
Vinci
Voltarelle
Vernie
139
632
643
568
604
638
V908I
V916F
V894G
V896F
V915F
V903D
F
M
M
M
F
F
Victoire
406
V896E
F
Volga
411
V916D
F
Tassadite
606
V893E
F
Gait
Age (yr)
Mass (kg)
2P
0.67
2.9
4P
0.55
2.7
2P
1.09
4.1
4P
1.09
4.1
2P
1.58
5.4
4P
1.88
6.1
2P
2.38
7.1
4P
2.39
7.1
2P
3.14
8.3
4P
3.27
8.5
2P
3.28
7.3
4P
3.12
7.1
2P
3.28
6.3
4P
3.15
6.1
2P
3.82
10.3
4P
3.63
9.9
2P
3.95
12.5
4P
4.09
12.5
2P
5.39
15.2
4P
5.09
14.5
Methods
The Motion Capture Setup The motion capture setup is based on a multicamera
high-speed video recording system. The recording zone is in the southeastern part of
the open-air enclosure B2F (Fig. 1). To guide the baboons along a regular path, we
built 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 m
long, 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 of
the 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 fence
on 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 the
observation area for 3D motion capture within a 2 m-wide field: 1 camera is
horizontally oriented, perpendicular to the long axis of the walkway, at a distance of
3.5 m from the center of the recording field and at a height of 40 cm above the top of
the 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 and
4.5 m distant from the centre of the recording field. The fourth camera is placed
opposite to the first camera, perpendicular to the long axis of the walkway, at a
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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.
distance of 9 m from the center of the recording field and covers a 4 m-wide field of
view. We use this camera to record longer sequences —walking, running, transitions,
jumping, etc.— and to make a posteriori measurements of speed variations over
several strides.
Each camera is connected to a workstation by means of 10-m long firewire cables
and an acquisition chart. The workstation is a purpose-built Streamstation. We
control the digital settings of the cameras, their synchronization, and the video
recording periods with Streampix 4.13.1 (Norpix). Synchronous recording by the 4
cameras 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 visualization
and store it as 4 separate sequences of equal sizes on the hard drive in the original
uncompressed software format (.seq). We then convert these sequences to AVI files
using motion analysis software, thanks to an automatic exportation procedure in
Streampix.
Bipedalism vs. Quadrupedalism in Olive Baboons
165
The Streamstation is set up in a wooden shelter built in line with the walkway
from which the movements of the baboons can be observed easily. We attract the
baboons 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 ≥2
complete walking cycles performed at constant speed at the subject’s own pace; we
selected bipedal gaits when the baboon’s hands were hanging free and it was not
carrying a load.
Owing to the baboon’s activity rhythm and the local climate, we made video
recordings from spring to autumn, preferably in the mornings. The winter break is
relatively short and does not cause significant gaps in the longitudinal monitoring of
immature 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 reference
points, of which we used 9 to construct a 6-linked segment model to analyze the
kinematics of the hind limb in a sagittal plane (Fig. 2a). We performed the entire
procedure 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-ray
imaging of individual 854 in a resting position (a) and the sagittal joint angles as calculated from these
anatomical landmarks (b).
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G. Berillon et al.
Kwon3D software (Visol). The 9 reference points are as follows: sagittally and
dorsally, the points corresponding to the base of the neck and the base of tail, and
then 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 plantar
points corresponding to the cuboid and the lateral metatarsophalangeal joint, and the
tip of the third toe.
Because the midfoot of a baboon is not rigid during the stance phase (Okada
1985; Meldrum 1991; Schmitt and Larson 1995), it was necessary to measure, as far
as technically feasible, the relative movements of the proximal tarsus on the lower
leg (taking place in the talocrural joint, essentially), and of the midfoot (the distal
tarsus and the metatarsus) against the proximal tarsus. This proved possible by
identifying ≥1 anatomical point between the talocrural joint and the metatarsophalangeal joint; both are classic reference points in the literature. Vereecke and Aerts
(2008) recently applied this principle to the highly compliant gibbon’s foot; they
used the tarsometatarsal joint on the assumption that motion essentially takes place
at this level, as proposed by recent experimental analysis (DeSilva 2010; Hirasaki
and Kumakura 2003); sagittal motion at the midtarsal joint level has already been
demonstrated for other locomotor modes such as leaping (Günther 1989). Our own
radiological observations and manipulations of cadavers and anesthetized individuals
confirm that foot compliancy occurs in the tarsometatarsal and transverse midtarsal
joints. For the moment, however, it is impossible to assess the relative importance of
the mobility of each joint, and to discern the exact position of these 2 joints in the
video recording. Therefore, as a first approximation, we selected the point located on
the plantar face of the foot corresponding to the intersection of the axis of the
proximal foot —represented by the plantar face of the heel— with the midfoot axis
represented by the plantar face of the metatarsus. We digitized this point directly in
the frames, where it appears to be located just behind the tuberosity of the fifth
metatarsal bone.
We transformed the 20 original sets of 2D coordinates into 20 calibrated sets of
coordinates, i.e., coordinates that are explained in a single common reference frame,
in this case based the walkway, for each sequence with the KwonCC calibration
procedure. 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 at
the beginning of each recording session. The DLT calibration procedure in the
KwonCC module produced an average reconstruction error of 0.79 mm.
Spatiotemporal Parameters and Joint Angles From the calibrated reference point
coordinates, we calculated absolute and dimensionless spatiotemporal parameters as
well as the joint angles of the lower limb following the procedure described in
Berillon et al. (2010). We computed the spatiotemporal parameters absolute stride
length (m), stride duration (s), stride frequency (s–1; we define a stride as one
complete gait cycle from touchdown of a foot to the next touchdown of the same
foot) and speed (m s–1), the duty factor, and dimensionless speed. We incorporated
available spatiotemporal parameters and values for hip and knee angles associated
with the bipedal gait (Berillon et al. 2010) into the full data set, including
quadrupedal spatiotemporal parameters, quadrupedal hip and knee joint kinematics,
and quadrupedal and bipedal joint kinematics of the foot. With regard to the foot
Bipedalism vs. Quadrupedalism in Olive Baboons
167
angles, in addition to the classical ankle joint angle, we computed the talocrural joint
angle, the metatarsophalangeal joint angles, and the midfoot angle (Fig. 2b). We first
present charts of the average movement over time, expressed as a fraction of cycle
duration, of the bipedal and quadrupedal hip, knee, and ankle joints and their
variation at key events in the complete cycle: maximum and minimum, local
maximum 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 movements
of the foot joints over time, expressed as a fraction of the stance phase duration. We
tested differences between bipedal and quadrupedal joint angles at gait events using
a covariance analysis procedure (ANCOVA, Statistica 6.0), with the joint angles as
dependent variable, the gait as independent variable, and the dimensionless speed as
covariate.
Results
Spatiotemporal Parameters
Table II shows individual and average values, SD, and the range of calculated
spatiotemporal parameters. During quadrupedal walking, the stance phase is
relatively short compared to bipedal walking, representing 66.4±0.3% of the cycle
duration (vs. 69.9±0.3% when the gait is bipedal); the stride length and stride
duration 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 angles
and their variations during bipedal and quadrupedal locomotion over time
expressed as a fraction of a cycle. Generally speaking, bipedal movements are
more variable than quadrupedal ones, in terms of values as well as the timing of
occurrences.
Considering the joints successively, we observed that the hip is always bent, but
significantly 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 during
quadrupedal locomotion. The peak of flexion is reached at ca. 58% of the cycle in
both modes, before the toe-off and shortly after contact of the opposite foot. The
total range of motion during a quadrupedal cycle (52.8°±4.8) is larger than during a
bipedal cycle (34°±7.1).
The knee is also always bent in the quadrupedal gait cycle, but significantly less
than in the bipedal gait. Minimum flexion is reached at initial foot contact and the
peak of flexion occurs at ca. 75% of the cycle in both modes, well after toe-off in the
quadrupedal gait cycle. The range of knee flexion is large but significantly smaller
during 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 initial
foot contact to the contralateral toe-off and 2) from the contralateral foot-contact to
its maximum, after toe-off; between both phases, knee flexion varies very little. In
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Table II Individual and average (mean±SD) lower leg length and spatiotemporal parameters
Individual
(medal)
Lower leg
length (m)
854
0.12
139
632
643
0.13
0.14
0.15
568
0.17
604
0.15
638
0.16
406
0.20a
411
0.19a
606
0.20a
Mean±SD
a
0.16±0.03
Gait
(2P/4P)
Stride
length
(m)
Stride
duration
(s)
Stride
frequency
(1/s)
Absolute
speed (m/s)
Dimension
less speed
Duty
factor
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
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
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
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
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
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
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
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
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
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
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
Calculated from video recordings.
bipedal locomotion, the knee flexion gradually increases from the initial foot contact
to its maximum. Finally, in both the bipedal and quadrupedal gait cycles, there is less
variation 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 follow
similar profiles and their values differ only slightly; in quadrupedal locomotion, the
values are significantly lower around the foot contact. Two main phases of extension
and flexion are separated by a peak of minimum flexion at toe-off. There is
remarkable variation in the time of the first peak of flexion, both in bipedal and in
quadrupedal gaits.
The Foot During the Stance Phase
We paid special attention to the foot during stance phase in both bipedal and
quadrupedal locomotions.
19.4±6.5
98.8±9.5
131.8±8.1
116.6±5.8
85.5±6.1
105.0±5.6
144.9±14.1
150.8±11.4
165.1±5.9 178.3±5.6 173.5±5.7
164.0±6.9 178.0±5.1 176.5±6.2
Metatarsophalangeal 2P
angle
4P
137.0±5.5
154.4±5.4 148.9±9.1 132.9±7.8
4P
137.5±7.8
99.5±7.2
105.0±8.0
93.5±9.2
149.0±3.6 136.2±8.2 128.8±6.6
97.1±7.3
114.2±4.8
4P
95.9±8.7
51.2±2.6
50.8±2.3
89.5±11.7 100.0±13.6
84.3±7.8
124.4±6.4 109.9±6.8 103.3±8.4
90.5±6.2
34.6±10.0
31.2±8.8
2P
119.6±8.0
112.4±9.1
2P
4P
124.8±6.6 102.9±5.8
134.5±3.9 117.7±2.9
2P
65.9±4.2
4P
59.1±4.0
104.8±9.8 110.2±8.3
16.4±2.6
Minimum
Opposite
ankle angle foot strike
2P
Midfoot angle
Talocrural angle
Ankle angle
Knee angle
4P
2P
4P
Hip angle
0±0
0±0
Time of occurrence 2P
Gait Initial foot Opposite
contact
toe off
69.9±3.4
66.4±2.3
65.6±2.6
67.5±4.2
119.6±7.1
149.5±7.1
156.6±8.1
119.6±7.4
150.5±7.7
146.7±10.1
153.5±12.9 137.3±10.5
149.5±7.4
156.7±7.7
118.2±6.3
117.0±10.5 119.9±11.0
118.7±6.5
86.9±6.4
63.7±8.8
76.5±2.0
74.7±3.1
162.2±4.8
179.4±27.4
145.5±6.8
144.4±4.2
95.1±5.6
103.6±6.7
90.1±7.3
100.8±7.6
83.1±3.2
84.3±3.4
Range of
motion
164.2±6.0
164.8±6.9
152.4±5.8
148.3±4.7
114.7±4.8
125.0±6.0
115.2±5.5
122.0±8.7
137.1±5.5
127.1±8.4
62.4±6.2
48.2±11.1
71.5±40.1
30.5±7.1
32.4±7.7
29.6±7.5
30.5±6.8
37.9±9.3
42.1±7.6
50.5±6.0
65.1±8.3
52.8±4.8
105.9±10.8 34.0±7.1
100±0
100±0
Maximum Minimum Final minimum Final foot
ankle angle knee angle ankle angle
contact
122.1±12.1 124.1±13.0
102.4±4.3
66.8±9.0
110.9±5.0 103.8±4.6
134.6±9.4 124.5±11.5
58.6±2.6
57.9±3.2
Maximum Toe Off
hip angle
Table III Time of occurrence of characteristic events of the stride (expressed as a fraction of cycle duration) and average angles at characteristic events (mean±SD)
Bipedalism vs. Quadrupedalism in Olive Baboons
169
170
G. Berillon et al.
Fig. 3 Comparison of mean changes of the hind limb angles and the events through a bipedal and a
quadrupedal 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 = quadrupedal
walking.
Type of Foot Contact with the Ground In most cases the foot touches the ground in
a rather horizontal position in both bipedal and quadrupedal gaits. It is placed
forward, in front of the hip; the knee and the ankle joint appear to be at their
maximum extension and plantarflexion respectively. We observed 3 main patterns
of foot contact with the ground (Fig. 4): 1) The foot comes into contact with the
ground 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 foot
is almost systematically observed immediately after the initial contact, but the heel
never touches the ground. This is the most frequent pattern in both gaits (7/10
quadrupedal and 8/10 bipedal). 2) The foot contact is initiated simultaneously by
the plantar surfaces of the midfoot and the toes; we observed this in the 2 youngest
subjects of the sample during bipedal locomotion (Ind. 854 and Ind. 139), and in 1
individual during quadrupedal locomotion (Ind. 638). 3) The foot contact is
simultaneously initiated by the plantar face of the heel and the midfoot and
0.0044
0.037
0.89
Metatarsophalangeal angle
0.167
Ankle angle
Midfoot angle
0
Knee angle
Talocrural angle
0.0016
Hip angle
Initial foot
contact
Table IV p values for ANCOVA analyses
0.327
0.014
0.002
0.009
0
0
Opposite
toe off
0.067
0.321
0.047
0.074
0
0
Minimum
ankle angle
0.574
0.789
0.126
0.268
0
0
Opposite
foot strike
0.588
0.78
0.461
0.732
0
0
Maximum
hip angle
0.305
0.043
0.92
0.255
0
0
Toe off
0.079
0.046
0.591
0.187
0
0
Maximum
ankle angle
0.107
0
0.024
0
0
0
Minimum
knee angle
0.067
0.321
0.047
0.074
0
0
Final minimum
ankle angle
0.491
0.258
0.001
0.031
0
0.038
Final foot
contact
Bipedalism vs. Quadrupedalism in Olive Baboons
171
172
G. Berillon et al.
Fig. 4 Lateral views of the 3 observed modalities of foot contact to the ground.
continues by the entire sole of the foot; this describes a plantigrade stance phase
with no heel-strike. Very soon after the initial contact, the proximal foot moves
upward. 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 of
bipedal 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 not
been described in the literature.
Pedal Joint Angles During the Stance Phase Table III and Fig. 5 show the changes
of average foot angles and their variations for bipedal and quadrupedal walking over
time expressed as a fraction of stance phase duration. Variation in the bipedal and
quadrupedal angles at each event is similar, in contrast to what is observed for the
ankle angle. The talocrural angle in both bipedal and quadrupedal gaits is >90°
during the stance phase, which means that the talocrural joint is kept slightly
extended; talocrural extension is at its maximum at the beginning and end of the
Bipedalism vs. Quadrupedalism in Olive Baboons
173
Fig. 5 Comparison of mean changes of the foot angles and the events through a bipedal and a
quadrupedal 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=quadrupedal
walking.
stance phase and reaches its minimum around midstance. The extension of the
talocrural joint is more pronounced in bipedal than quadrupedal mode, and
significantly so during the first half of the stance phase (Table IV). The midfoot is
bent dorsally concave, with flexion at its maximum at approximately midstance.
This flexion is significantly higher in a bipedal gait cycle at the beginning of the
stance phase. This tendency is then progressively reversed, with the midfoot
significantly more bent during the quadrupedal gait at toe-off. Thus, at the beginning
of the stance phase of a bipedal gait cycle, the proximal foot is raised in a relatively
more elevated position than in quadrupedal locomotion. We observed no significant
difference between the bipedal and the quadrupedal profiles of the metatarsophalangeal joints. After a short period of dorsiflexion at the initial contact, this joint
quickly reaches its neutral 180° position. On average, during the second half of the
stance phase, the joint dorsiflexes up to a peak at the end of the stance phase, with
dorsiflexion then decreasing at toe-off. These average profiles illustrate a general
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G. Berillon et al.
increase in the dorsiflexion of the tarsometatarsal complex during the first half of the
stance phase; this movement is then reversed while the metatarsophalangeal joints
starts dorsiflexing.
To understand the variation observed, we now focus on the way the joints of
the individual study subjects behave (Fig. 6). In general, for each type of
locomotion, we observed that individual movements follow a rather similar pattern
but the relative duration of the different periods varied widely among the individuals
in the sample. The foot kinematics during the bipedal stance phase can be described
as follows:
&
&
The touchdown period: The metatarsophalangeal dorsiflexion quickly returns
from 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 midfoot
increases 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) stance
phase.
Bipedalism vs. Quadrupedalism in Olive Baboons
&
&
175
individuals. No movement occurs at the metatarsophalangeal joint. At the end of
the loading period, the plantar surface of the proximal tarsus is in an elevated
position.
The tarsometatarsal rise period: The metatarsophalangeal joint dorsiflexes
leading to a regular lifting of the tarsometatarsal segment; simultaneously, the
dorsiflexion of the talocrural joint and the midfoot decreases. The peak of
maximum metatarsophalangeal dorsiflexion and the peaks of minimum talocrural
and midfoot dorsiflexion are reached simultaneously at 85–95% of the stance
phase.
The push-off period: The metatarsophalangeal dorsiflexion quickly decreases
while 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 midfoot
moves in the opposite direction; the dorsiflexion of the metatarsophalangeal joint
lessens 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 the
midfoot dorsiflexes. The metatarsophalangeal joint remains in its slightly extended
position. The peak of maximum midfoot flexion is reached at the moment when
metatarsophalangeal 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 of
minimum (for the talocrural joint and the midfoot) and maximum (for the
metatarsophalangeal joint ) dorsiflexion are reached at 85–95% of the stance phase.
The push-off period: the metatarsophalangeal dorsiflexion quickly lessens while
the talocrural joint and the midfoot begin a second phase of dorsiflexion.
Individual variation is important, as highlighted by the characteristics of the
touchdown to tarsometatarsal rise periods of individual 139 in quadrupedal locomotion.
Although touchdown is immediately followed by a rapid decreasing of the
metatarsophalangeal dorsiflexion until it reaches its neutral position, which is observed
in all other individuals of our sample, it is as well immediately followed by a
dorsiflexion of the midfoot. In the other individuals, the dorsiflexion of the midfoot
remains constant or more often decreases, at this time of the stance phase. In addition,
the metatarsophalangeal joint, after reaching its neutral position, immediately
dorsiflexes until it reaches its maximum. This dorsiflexion is usually initiated later in
the other individuals, whereas almost no motion occurs at the talocrural and midfoot
level during that period.
To summarize, the kinematics of the talocrural joint, the midfoot and the
metatarsophalangeal joints act in a coordinated manner, but are triggered differently
according to whether the support is bipedal or quadrupedal. In bipedal locomotion,
the tarsometatarsal complex dorsiflexes gradually as soon as the foot touches the
ground, while in quadrupedal locomotion, the stance phase starts with a decreasing
of the midfoot dorsiflexion; as a consequence, the posterior foot slightly collapses at
the initiation of the quadrupedal touchdown. We did not observe this difference at
the ankle kinematics level; this could be explained by the method of measuring the
ankle angle, which combines both talocrural and midfoot kinematics.
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G. Berillon et al.
Discussion and Conclusion
Baboons are conventionally described as committed quadrupedal primates (Fleagle
1988; Rose 1973). They are also known to occasionally and spontaneously walk
bipedally (Hunt 1989; Rose 1976, 1977; Wrangham 1980). However, precise
kinematics of both locomotor modes remain rare and include few individuals (Ishida
et al. 1974; Okada 1985; Shapiro and Raichlen 2005). As far as lower limb and foot
kinematics and stance phase descriptions are concerned, a total of 4 individuals have
been observed (Meldrum 1991; Okada 1985; Schmitt and Larson 1995). We are
currently documenting movements of unrestricted animals and testing their mobility
in passive manipulation and X-ray imaging. We have provided original data from an
initial sample of 10 Papio anubis, focusing here on lower limb and foot kinematics
in bipedal vs. quadrupedal locomotion. We describe the trunk and hind limb bipedal
kinematics elsewhere (Berillon et al. 2010).
As far as the foot stance phase is concerned, Okada (1985) noted that bipedal and
quadrupedal locomotor modes were very similar and of semiplantigrade type for 1
individual (Papio hamadryas). This type of semiplantigrade foot contact was also
highlighted for 3 other baboons (1 Papio ursinus and 2 Papio anubis) in
quadrupedal locomotion (Meldrum 1991; Schmitt and Larson 1995). Our observations of a larger sample in both bipedal and quadrupedal locomotion demonstrate a
variety of foot contacts, from semiplantigrady, which we observed most frequently
in our sample, to full-fledged plantigrady, observed only in quadrupedal
locomotion.
Our qualitative observations are supported by the data concerning foot kinematics
during the stance phase.The multisegment anatomical model allows a quantitative
decomposition of both bipedal and quadrupedal stance phases at an individual level.
This approach is based on observations of midfoot flexibility in many nonhuman
primates, 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; Gebo
1992; Günther 1989; Meldrum 1991; Schmitt and Larson 1995; Vereecke and Aerts
2008; Vereecke et al. 2005). Researchers have evaluated this midfoot flexibility
anatomically (Bojsen-Moller 1979; Lewis 1989), although some have challenged its
anatomical origin (Günther 1989; DeSilva 2010). In several analyses of bipedal and
quadrupedal hindlimb kinematics of nonhuman primates, researchers have modeled
the 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 relate
to the available recording tools: relatively low speed and resolution recording did not
provide frames of sufficient quality that would allow digitization of landmarks other
than the usual, well-identified ones. In addition, as far as the evolution of the ankle
joint angle through a stride is concerned, one can make a direct comparison with
humans. Okada (1985) was the first to propose a quantified kinematic analysis of the
compliant foot, based on the virtual division of the foot into several “blocks”. This
study was very innovative, although its approach might not be trivial to implement
in a highly reproducible manner. More recently, Vereecke and Aerts (2008) proposed
an approach using high-speed video sequences and their analysis based on the
identification of anatomical referenced points for gibbons (Hylobates lar): they
calculated the position of the tarsometatarsal joint from highly reproducible external
Bipedalism vs. Quadrupedalism in Olive Baboons
177
referenced points via a triangulation procedure, assuming that the flexion mainly
occurs 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, our
manipulations of captured and anethesized individuals of the sample and of cadavers
showed that nonnegligible motion occurred at both the transverse midtarsal joint and
the metatarsophalangeal joint level, although it was not possible to measure their
relative importance at this stage. Unfortunately, we could not identify these 2 joints
on the video sequences by proper external reference points. We thus chose to build a
point at the midfoot level that represents the intersection of 2 visible axes, those of
the proximal foot and of the metatarsus. The angle thus represents the total flexion
that 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 stance
phase in gibbons and that “this midfoot dosiflexion will stretch the tendons and
ligaments running across the plantar side of the foot, potentially storing elastic
energy and eventually contributing to propulsion generation at push-off.” In olive
baboons, we show that the dorsiflexion of the midfoot increases from the touchdown 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 the
ground. Could this mechanism potentially contribute to storing elastic energy?
Kinetics for baboons must be measured to evaluate this point. Nevertheless, we
observed 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 during
the bipedal gait in baboons.
Because baboons are highly adapted quadrupedal primates, one could expect that
quadrupedal kinematics, especially at the foot level, would be less variable than
those of the less frequently used bipedal locomotor mode. D’Août et al. (2004) used
this hypothesis to explain the higher variability in bipedal vs. quadrupedal hindlimb
kinematics in the bonobo. Although bipedal kinematics of the hip and knee are more
variable than those in the quadrupedal locomotion of olive baboons, our data do not
support this hypothesis due to the similarity in variation for bipedal and quadrupedal
foot kinematics. Moreover, our analysis of the individual joint angle trajectories
demonstrates that joint kinematics are synchronized for both bipedal and
quadrupedal locomotion; they follow very similar modalities from one individual
to the other but the timing is very variable. Finally, significant differences between
bipedal and quadrupedal kinematics of the talocrural joint and the midfoot exist. In
particular, in quadrupedal locomotion the stance phase is initiated by a phase of
decreasing of the midfoot dorsiflexion. Thus, it seems that motions involved in
bipedal and quadrupedal locomotions of olive baboons act in 2 well-coordinated and
stereotyped manners.
Terrestrial bipedal walking in baboons must be seen as a proper and not erratic
locomotor 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 very
early hominids, in which terrestrial bipedalism should be seen as a usual locomotor
modality, although their anatomy retained several or many traits that would fit better
to arboreal habits (Senut et al. 2001; White et al. 2009).
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G. Berillon et al.
Acknowledgments We thank the editors of this volume and organizers of the symposium on Functional
Morphology in Primates in Durham for inviting us to introduce our ongoing program on baboon
locomotion; this contribution is based on this introductory presentation. We also thank the other members
of the Primatology Station, especially Valérie Moulin, for her permanent help. The entire motion capture
system was set up with the collaboration of P. Trannois (Opto France, France); the Streamstation was
configured with the help of T. Lemaire. This research is supported by the Fyssen Foundation (Research
Grant), 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 on
previous versions of the manuscript as well as Joanna M. Setchell, who contributed to the revision of the
English and the editing of the final version of the manuscript.
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