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First published online November 14, 2008
Journal of Experimental Biology 211, 3661-3670 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018754
The mechanics of the gibbon foot and its potential for elastic energy storage during bipedalism
1 Department of Human Anatomy and Cell Biology, School of Biomedical Sciences,
University of Liverpool, Liverpool L69 3GE, UK
2 Laboratorium for Functional Morphology, University of Antwerp,
Universiteitsplein 1, B-2610 Antwerp, Belgium
3 Department of Movement and Sports Sciences, University of Ghent,
Watersportlaan 2, B-9000 Gent, Belgium
* Author for correspondence (e-mail: evie.vereecke{at}liv.ac.uk)
Accepted 30 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: biomechanics, energy-saving, mechanism, human evolution, joint movements, kinematics, primate locomotion
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Wolde Gabriel et al., 2001;
Madar et al., 2002;
Senut, 2003;
Senut, 2006;
Pickford, 2006) indicate that
our early ancestors were tree-dwelling apes, and several evolutionary models
(Stern, 1975;
Prost, 1980;
Tuttle, 1969;
Tuttle, 1981;
Senut, 2003;
Senut, 2006;
Clarke, 2003;
Pickford, 2006) suggest
bipedalism arose in this particular environment. The most recent model, based
on observations of extended-leg bipedalism in wild orang-utans and supported
by the fossil record (Thorpe et al.,
2007; Crompton et al.,
2008), suggests that habitual terrestrial bipedalism derived from
arboreal hand-assisted bipedalism in a habitually orthograde hominoid. This
ancestral orthogrady model (Crompton et
al., 2008) is further supported by Filler
(Filler, 2007), who found that
a mutation(s) in homeobox genes governing lumbar vertebra morphology and
facilitating habitual orthogrady, may have been present in our hominoid
ancestors. This may well put back the origin of habitual bipedalism to earlier
dates than currently held. The nature of this ancestral bipedal gait is still
debated, but whether it was bent-hip, bent-knee (like gibbons and bonobos)
(D'Août et al., 2002;
Vereecke et al., 2006a) or
stiff-legged (like orang-utans) (Thorpe et
al., 2007), it was certainly executed with a relatively mobile,
prehensile foot, and not with a foot like that of modern humans.
The modern human foot is highly specialized for terrestrial bipedalism. It
has several unique characteristics, such as an enlarged calcaneal tuberosity,
stabilized calcaneocuboid and talonavicular joints, a longitudinal arch and
strong plantar aponeurosis (Harcourt-Smith
and Aiello, 2004; Klenerman
and Wood, 2006), all of which constitute the typical mechanical
behaviour of the human foot during bipedalism. One of the most recognized
features of the modern human foot is its ability to change from a compliant
shock-absorber at heel-strike to a rigid lever at toe-off by supination of the
subtalar joint (Donatelli,
1996). Further midfoot stabilization results from hallux
dorsiflexion, tightening the plantar aponeurosis and offering the required
stability for propulsion at push-off. This principle is known as the windlass
mechanism (Hicks, 1954;
Gershman, 1988;
Fuller, 2000). In addition,
the arched foot also enhances the efficiency of bipedalism by storage and
release of elastic strain energy in the plantar aponeurosis
(Ker et al., 1987). This dual
function makes the modern human foot particularly well adapted for
terrestrial, bipedal walking and running.
However, fossil evidence suggests that a truly `modern' configuration of
the human foot is a quite recent phenomenon, which evolved after the
appearance of early Homo (approx. 1.8 Ma)
(Kidd et al., 1996;
Bramble and Lieberman, 2004;
Harcourt-Smith and Aiello,
2004; Klenerman and Wood,
2006; Crompton et al.,
2008), probably linked to long distance walking/running in a
drier, more open environment. Some modern human-like features, such as an
adducted hallux, increased metatarsophalangeal dorsiflexion and midfoot
stabilization, may be found in earlier (5–2 Ma) hominin foot bones (see
Harcourt-Smith and Aiello,
2004; Klenerman and Wood,
2006), but these traits are not all present in any single early
hominin foot, and combined with `arboreal' characteristics, leading to a
`mosaic' foot structure with considerable mobility
(Stern and Susman, 1983)
(reviewed by Crompton et al.,
2008). This implies that the adoption of a partially terrestrial
bipedal gait – evidenced by the Laetoli footprints at 
3.5 Ma but
possibly occurring as early as 6–7 Ma
(Pickford et al., 2002;
Richmond and Jungers, 2008)
– predates the evolution of a specialised bipedal foot. Thus, our early
hominin ancestors (>5 Ma) probably retained a relatively mobile and
essentially flat foot structure, though frequently or even habitually,
engaging in terrestrial bipedalism. This might mean that their behaviour still
included arboreal activities (for which a mobile foot is advantageous), and/or
that selective pressures for a terrestrially specialized foot were low. Though
we might not yet fully understand the different evolutionary stages that led
to the configuration of the modern human foot (mainly because of a lack of
fossil foot bones) (Harcourt-Smith and
Aiello, 2004), we can make inferences about the foot function of
protohominins by studying the form and function of the foot in extant
apes.
As an evaluative proxy for the foot function of protohominins, we have studied the foot function of untrained gibbons during terrestrial bipedal locomotion. Note that we are not claiming that gibbons are the best model for protohominins, nor that the architecture of the protohominin foot was similar to that of extant gibbons (claims which would be unsupported by fossil findings). Yet, the high mobility of the gibbon foot as well as the arboreal lifestyle and regular display of both arboreal and terrestrial bipedalism, makes the gibbon a valuable model for an ancestral tree-living hominoid/protohominin.
Gibbons are the most bipedal of all nonhuman primates, with bipedalism
accounting for 10–12% of their locomotor activities
(Cannon and Leighton, 1994).
Gibbons alternate brachiation with fast bipedal bouts on large boughs and
branches (diameter >10 cm) (Fleagle,
1976; Gittins,
1983), and bipedalism is their preferred terrestrial gait (more or
less imposed by their long arms) when crossing gaps in the forest canopy
(Sati and Alfred, 2002). This
means that, despite the high incidence of brachiation, the hind limbs are
important for propulsion generation in gibbons. Like most arboreal primates,
gibbons have a mobile, prehensile foot structure with a divergent, opposable
hallux. The gibbon foot is essentially flat (i.e. lacks a longitudinal arch as
seen in modern humans) and displays a midtarsal break during bipedalism
(Vereecke et al., 2003;
DeSilva and MacLatchy, 2008).
The plantar aponeurosis is relatively weakly developed compared with the human
plantar aponeurosis (Vereecke et al.,
2005b); however, other plantar connective tissues lying deep to
the plantar aponeurosis, such as the plantar ligaments and the tendons of the
digital flexors, are prominent (Vereecke
et al., 2005b). Both the long digital flexors and gastrocnemius
are short-fibred, pennate muscles, favouring economical force production and
elastic energy usage. Unlike other nonhuman apes, the external portion of the
gibbon Achilles' tendon (i.e. triceps surae tendon) is particularly long,
comparable in size to the human Achilles' tendon. A diagram of potential
elastic energy stores in the gibbon foot is given in
Fig. 1.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) are combined with detailed foot kinematics (this study) to
calculate the external joint moments at the metatarsophalangeal,
tarsometatarsal and talocrural joint during the stance phase. In addition,
instantaneous joint power and external work are determined to obtain insight
into the propulsion-generating capacities of the internal foot joints.
It must be emphasized that, in accordance with zoo policy, all bouts were
collected without any direct interaction with the subjects. Though this
ensures that all recorded bouts represent spontaneous bipedal walking, this
constraint made data collection (since our camera was zoomed in on an area of
45 cmx45 cm, halfway along the wooden walkway) and analysis (manual
digitization was necessary since subjects were unmarked) much more complicated
and limited the number of successful trials that could be included in the
analysis. Furthermore, practical considerations inherent to working with
untrained animals in an unrestrained zoo environment meant that neither the
setup in the present study, nor that used in an earlier force and pressure
study by Vereecke et al. (Vereecke et al.,
2005a) allowed for simultaneous recording of high-speed video and
force/pressure measurements. Therefore, external joint moments were calculated
by combining the registered point position data (collected in this study) with
available force and plantar pressure data that had been collected
simultaneously in a previous study
(Vereecke et al., 2005a) using
an AMTI force plate (Watertown, MA, USA) and a Footscan pressure mat (RSscan,
Olen, Belgium).
Data acquisition
Sagittal joint motion was recorded during spontaneous bipedal locomotion of
a group of white-handed gibbons (Hylobates lar, Linnaeus). Recording
equipment was installed in the outdoor gibbon housing of the Wild Animal Park
Planckendael (Belgium) and consisted of a high-speed MotionPro video camera
(RedLake, Tucson, AZ, USA), set at sampling rate 250 Hz and shutter gate 1/500
s, mounted on a tripod, and positioned perpendicular to a 2 m-long wooden
walkway and a 1 m-high wall reference-marked with a 0.1 cmx0.1 cm grid.
The walkway was aligned orthogonally opposite a gateway to the indoor
enclosure to enhance the frequency of spontaneous bipedal bouts, since no
direct interaction with the animals was allowed by the zoo protocol. We
collected a total of 68 bipedal bouts from three adult gibbons. All 68 records
were used for qualitative evaluation and no apparent differences were observed
in the footfall pattern and bipedal gait of the different individuals. For
detailed analysis we have focused on recordings of a young male subject (6
years old; mass 6.3 kg) since owing to death from natural causes we were able
to collect required anatomical data post-experimentally, and since ground
reaction force profiles and plantar pressure distributions were available for
this individual from a previous study
(Vereecke et al., 2005a).
Eight bipedal bouts of this individual were selected based on steadiness of
overall walking speed (no apparent acceleration or deceleration), foot
placement and stance phase duration. Only bouts with a stance phase duration
between 0.50 and 0.65 s (corresponding to a speed range of 0.7–1.0
m s–1) and a nearly parasagittal (slight toe-out) foot
position were retained. Comparison with digitized sequences of each of the
other individuals indicated that the foot kinematics of the eight selected
trials of the young male subject were indeed representative of the species'
foot motion pattern. Quantitative foot motion data is presented only for this
young adult male, but a figure of the footfall pattern of all three gibbons is
provided to show the similarity in foot motion
(Fig. 4).
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)
to analyse the 2D motion of the talocrural, tarsometatarsal and
metatarsophalangeal joints in the parasagittal plane. The different segments
were defined by digitization of the following locations
(Fig. 2): toe (T),
metatarsophalangeal joint (MP), tarsometatarsal joint (TM), heel (H),
talocrural (TC) and knee joint (K). Although these measurements were performed
manually on each frame, the high resolution (1280 pixelsx1024 pixels) of
the full-frame video images enabled accurate digitization of the various
points. To test repeatability of digitization, we digitized one sequence four
times and calculated the standard deviation of the point positions. The
standard deviation of the T, MP, TC, H and K position was 4 mm, but, the
standard deviation of the TM position amounted up to 6 mm. We therefore
decided to determine the TM position using our knowledge of the subject's foot
osteology – taken from the subject which had died after filming –
rather than using manual digitizations. We used a Matlab routine (Matlab 7.2
for Windows) to calculate the position of the tarsometatarsal joint (TM) from
the position of the heel (H) and talocrural joint (TC), based on the
assumption that the hindfoot, enclosed by TC–TM–H, is a rigid
triangle with known sides (see also Fig.
2). The length of the sides (TC–TM=26 mm, TC–H=35 mm,
H–TM=39 mm) was obtained from measurements of the articulated foot
skeleton of the deceased subject. This calculated position of the TM was used
in all further analyses.
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The raw positional data were filtered using a fourth order Butterworth
low-pass filter with 7 Hz cut-off frequency in Kwon3D. This was the optimal
cut-off frequency, which was determined using residuals against frequency
plots of the positional and angular data as described by Winter
[(Winter, 1990) pp.
41–43]. In order to obtain the transformation parameters we digitized
six points on the grid (0.2 mx0.1 m) of the reference wall in five
consecutive frames of the camera view. An additional point, set at the tip of
the toes, was used to translate the coordinate axes to the toe, T (0, 0). This
calibration was done for each sequence because the camera position could
change from sequence to sequence. Calibration was performed using the 2D-DLT
Algorithm in KwonCC 3.01 for Windows
(Kwon, 1994) and yielded a
reconstruction error of 0.3–0.5 mm.
For generation of average point position data (x, y coordinates of
T, MP, TM, TC and K) we resampled each sequence to comprise exactly 51
intervals of 2% stance phase duration (linear interpolation within the
boundary measuring interval was applied; LabVIEW 8 for Windows). For each 2%
interval the average point position (x, y coordinates; N=8)
was calculated, and combined with the average forces
(Fx, Fy) and centre of
pressure (COPx) data [taken from Vereecke et al.
(Vereecke et al., 2005a)]
which were also resampled to 51 intervals of 2% stance duration (see below). A
Matlab routine was used to create stick figures of the position data and plot
the force vector (see below for origin of force information) over a full
stance phase.
Joint angles
We computed three two-dimensional joint angles, at the talocrural (TC),
tarsometatarsal (TM) and the metatarsophalangeal (MP) joints, from the point
position data using basic trigonometry (Excel for Windows). The joint angles
were defined as the angles between two adjacent segments, as illustrated in
Fig. 2B. An increase in joint
angle indicates joint plantarflexion; a decrease points to dorsiflexion. The
joint angles were calculated for each sequence based on the resampled point
coordinates (51 intervals) and the average joint angle of the eight sequences
(± standard deviation) was plotted as a function of time.
External joint moments
The present dataset was carefully aligned with average force and pressure
profiles from a previous study (Vereecke
et al., 2005a). Integration of the force/pressure measurements and
kinematics was performed by resampling each data set to 100% stance phase
duration. Furthermore, in order to enable alignment of both data sets, the
same reference frame, a right handed coordinate system with the toe as origin,
was used. In Vereecke et al. (Vereecke et
al., 2005a), the instantaneous centre of pressure (COP) was
recorded using an RSscan pressure mat, installed on top of an AMTI force
plate, and Footscan software was used to export the fore–aft coordinates
of the COP (COPx) during the full stance phase duration.
We calculated the average vertical (Fy) and
horizontal (Fx) force profile and the average path
of the centre of pressure (COPx; fore–aft component)
for a series of bipedal sequences within the same speed range
(0.7–1.0 m s–1), a nearly sagittal foot placement
and performed by the same gibbon as the kinematic data collected in the
current study.
Masses – and hence moments of inertia – of the foot segments
are small; the total mass of the foot accounts for only 1.2% of the total body
mass. This, combined with the limited linear and angular displacements (and
hence accelerations) involved during stance, allowed for a static approach
neglecting gravity and inertia. We computed the moments at the MP, TM and TC
joint using a trigonometric method [cf. the FRFV approach of Winter
[(Winter, 1990) pp.
92–93] (see also Biewener,
1983; Biewener,
1998; Hansen et al.,
2004)]. As shown previously
(Wells, 1981;
Winter, 1990;
Vaughan, 1996;
Simonsen et al., 1997;
Hansen et al., 2004) joint
moments calculated with this method for the human ankle (and internal foot)
joints, are very similar to those obtained from inverse dynamics calculations
taking inertia and gravity into account.
For each 2% interval, this method calculates the moment arm (MA) of each
joint (i.e. the perpendicular distance between the joint centre and the line
of action of the resultant ground reaction force vector; GRF), which is then
multiplied by the magnitude of the force vector
[GRF=
(Fx^2+Fy^2)]
to yield the external joint moment. The sign of the external joint moment was
defined according to the relative position of the x-coordinate of the
MA–GRF intercept; when lying proximal to the joint (i.e. a smaller
x-coordinate than that of the joint) it was considered negative
(dorsiflexor moment), when distal to the joint (i.e. having a larger
x-coordinate than that of the joint) it was considered positive
(plantarflexor moment). The use of the trigonometric method with application
of the resultant GRF at the COPx is in fact only justified for joints proximal
to the point of application of that resultant force vector. However, from
pressure distribution patterns (Fig.
3) (Vereecke et al.,
2005a) it is obvious that foot segments situated distally to the
one on which the resultant force applies (i.e. the location of the
COPx) are never loaded to a significant extent. This means
that moments at joints distal to the COPx are virtually
zero (only gravity is in play). In practice, reliable estimates of joint
moments can therefore be made for all foot joints throughout foot contact.
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Instantaneous joint power and external work
To estimate the potential elastic storage of energy in the triceps and
digital flexors, we calculated instantaneous joint powers and positive and
negative external work at each joint. The instantaneous power was obtained for
each joint by multiplying joint moment (in N m) by angular joint velocity (in
rad s–1) during the stance phase. The joint moment and
angular velocity used in these calculations are instantaneous values computed
as averages of the joint moments and angular velocities occurring in the eight
bouts. The instantaneous joint power was plotted as a function of stance phase
duration (using a 12 ms time interval, corresponding to the previous 2%
intervals), and the power–time integral was calculated to obtain
positive and negative external work performed at each joint. Total foot power
was also calculated, by summing the instantaneous joint powers of the MP, MT
and TC joint, as well as positive and negative external work occurring at foot
level. In this way potential energy transfer via multi-articular
muscles and ligaments is considered.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The touchdown phase (0–10% stance phase)
Initial contact is made with forefoot or hallux, resulting in maximal ankle
plantarflexion. Loading remains relatively low (<0.5 body mass;
Mb).
The loading phase (10–50% stance phase)
During this predominantly braking phase (demonstrated by a negative
horizontal force component, Fx; cf. the posteriorly
oriented GRF in Fig. 5B and
Fig. 6), loading rises steadily
until maximal weight bearing is achieved (1.3 Mb).
Peak pressures are located near the base of metatarsal V and the navicular
bone (Fig. 6). Both the ankle
and TM joint dorsiflex continuously, while no substantial motion occurs at the
MP joint. The ground reaction force vector (GRF) is located distal to the TM
joint (at metatarsal segment; Fig.
5B, Fig. 6).
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The push-off phase (75–100% stance phase)
While loading drops (<0.8 Mb; unloading), the force
shifts further forwards now leading to (small) peak pressures under the
phalanges (Fig. 5D,
Fig. 6). This phase is denoted
by marked MP dorsiflexion (hyperextension) followed by MP plantarflexion,
while the ankle and TM joint plantarflex until toe-off.
It should be noted that because of a high step-to-step variability in gibbons, the characteristics of these four phases can differ slightly between individuals and between steps. For example, in Fig. 4 it can be seen that during the loading phase the foot can either have a heel-down or a heel-elevated position, though the latter was only observed sporadically.
Joint angles
The MP joint remains in a neutral (180 deg.) or slightly flexed position
throughout the first 80% of the stance phase, while there is a variable degree
of dorsiflexion at the TM joint (Fig.
7). Heel rise is associated with dorsiflexion at the TM (and TC)
joint, so that the forefoot remains in contact with the substrate while the
heel is off the ground. This heel rise event is followed by dorsiflexion at
the MP joint (around 75% of the stance phase), and TM joint
plantarflexion.
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80% of the stance phase (apart from some initial plantarflexion) as the
tibia rotates over the foot (Fig.
5). The total range of motion at the TC joint averages 71 deg.
during the stance phase. The TC joint plantarflexes slightly during the last
20% of the stance phase and continues to plantarflex during early swing.
External joint moments
The joint moments at the TC and TM joint are positive throughout the stance
phase, pointing to a continuous plantarflexor moment
(Fig. 7). This results from the
fact that the GRF vector runs anterior to both joints at all times
(Fig. 5), forcing the joints
into dorsiflexion and leading to a counteracting plantarflexor moment
presumably generated by the plantarflexor muscles (triceps surae and long
digital flexors). As explained before, virtually no moments occur at the MP
joint as long as the phalangeal segments remain unloaded (Figs
3 and
5). Therefore, only during the
last 20% of the stance phase, when the phalanges are clearly loaded, do we
observe a (positive) plantarflexor moment at the MP joint, presumably
generated by the long digital flexors and intrinsic plantar foot muscles.
Instantaneous joint power and external work
Although the external joint moments indicate to a certain extent which
muscle groups (flexors, extensors) are active, net joint moments cannot reveal
co-contractions and antagonists. However, net joint powers and external work
can be used to gain insight into the manner in which these muscle groups
function throughout the contact phase of the step cycle: generating or
absorbing mechanical energy (i.e. concentric versus eccentric
contractions). In addition, it allows us to evaluate the potential for elastic
energy storage in the muscle–tendon units crossing these joints.
Instantaneous joint power and external work performed at each joint are
presented in Fig. 8.
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However, whereas the triceps only crosses the TC joint, the long digital flexors cross the TC, TM and MP joint and the short digital flexors cross both the TM and MP joint (see Fig. 1). This anatomical configuration means that energy transfer via the digital flexors is possible across the three joints. To account for this, we have added up the power profiles of the three joints (Figs 8 and 9). The estimated external work performed at foot level amounts to –2.43 J during the first 80% of the stance phase and +0.78 J during the last 20%. Scaled to body mass (6.3 kg) and average stride length (0.65 m), this gives –1.25 J kg–1 m–1 energy absorption and +0.20 J kg–1 m–1 energy output.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) [cf.
humans (Belli et al., 2002;
Hansen et al., 2004)] –
despite some abduction/adduction and pronation/supination – and the
combined rotations of the digits at the TM and MP joints also occur about a
near-transverse axis.
Foot joint mechanics during bipedalism
Gibbons have a very flexible foot structure, where a passive range of
motion of 150 deg. at the TC and MP joints can be demonstrated by
manipulation of cadaveric feet (personal observation). This high joint
mobility is definitely related to their habitual locomotor and postural
behaviour. Wild gibbons are confined to life in the trees, and the mobile
ankle and foot joints provide the agility needed to adjust to the varying
inclination, orientation and size of branches in this complex 3D environment
(Gebo, 1993). The long, curved
toes, abducted hallux, strong flexors and mobile tarsal joints of the gibbon
foot facilitate a powerful grip, which is beneficial during climbing,
clambering and quadrumanous hanging
(Fleagle, 1999). As one would
expect, this mobility is also present during bipedalism (see also Fig. S1 and
Movies 1 and 2 in supplementary material), and means that the gibbon foot
cannot act as a rigid lever during push-off. This high foot mobility also
underlines the importance of using a multi-segment foot model in the analysis
of gibbon, and ultimately primate, locomotion.
Despite the larger angular excursion of the TC and TM joints in gibbon (71
deg. and 38 deg., respectively) compared to human bipedalism (15–25 deg.
and 10–15 deg., respectively), the shape of the joint angle profiles is
largely similar in both species (Kidder et
al., 1996; Carson et al.,
2001; MacWilliams et al.,
2003). The TC and TM joints dorsiflex during the first 80% of the
stance phase and plantarflex during the last 20%
(Fig. 7). In gibbon bipedalism
there is no initial TC plantarflexion, however, as gibbons touchdown with the
forefoot (hallux or metatarsal heads; Fig.
4) and not with the heel, like other apes and humans (i.e. absence
of a heel-strike) (Schmitt and Larson,
1995; Vereecke et al.,
2005a). As soon as the digits touch down the tendons of the long
digital flexors will be stretched since the long digital flexors are
relatively short muscle tendon units in gibbons (passive extension of the
digits is only possible when the TC joint is plantarflexed and TC joint
dorsiflexion is coupled with flexion of the digits). Thus, eccentric work and
potential energy storage at the TC and TM joints can start from initial
contact. This tightening of the tendons of the long digital flexors might also
be responsible for the coupling of TM plantarflexion and MP dorsiflexion in
late stance, something which is also observed in human gait
(Carson et al., 2001).
Dorsiflexion at the MP joint is, however, more pronounced in humans than in
gibbons: 35–45 deg. vs 28 deg.
(Kidder et al., 1996;
Carson et al., 2001;
MacWilliams et al., 2003).
This marked toe dorsiflexion is a typical feature of human gait, reflected in
the dorsal expansion of the MP joint articulation, and plays an important role
in the windlass mechanism (i.e. tightening of the longitudinal foot arch by
winding the plantar fascia around the metatarsal heads)
(Gershman, 1988;
Fuller, 2000).
The joint moment profile of the TC joint during gibbon bipedalism, and
specifically the plantarflexor moment during the entire stance phase duration,
corresponds to previous results reported by Ishida et al.
(Ishida et al., 1976). It is
similar to the human pattern but is considerably smaller in magnitude when
scaled to body mass and foot length (0.29 in gibbons vs 0.54 in
humans). Ishida et al. (Ishida et al.,
1976) suggested that the presence of a plantarflexor moment prior
to toe-off points to an active push-off in gibbons, a finding supported by
their EMG results showing maximal activation of the triceps surae during late
stance (see also Okada and Kondo,
1982). However, their EMG data show that during gibbon bipedalism
the long digital flexors are also active throughout stance. Combined with our
results, this suggests that, during late stance, co-contraction of the triceps
and long digital flexors will lead to plantarflexion at both TC and TM joints,
generating propulsion for push-off. Contraction of the digital flexors will
also lead to plantarflexion at the MP joint during the last 10% of stance, but
given the small plantarflexion moment the contribution of the MP joint to
propulsion will be small.
Potential for elastic storage
Instantaneous joint powers were calculated to get insight in the function
of the recruited muscle groups during the stance phase. The results show that
during the first 70–80% of the stance phase, the plantarflexor muscles
work eccentrically, potentially loading the well-developed Achilles' tendon,
long digital flexor tendons and connective tissue components of the plantar
foot (cf. Vereecke et al.,
2005b) with elastic energy. This is followed by concentric
contraction of the plantarflexor muscles during late stance. The amount of
positive external work performed at the TC and TM joint is similar, and is
preceded by generation of negative external work at both joints
(Fig. 8). To estimate how much
of this positive external work could come from elastic recoil, we compared the
relative amounts of negative and positive work at both joints during stance.
We took account of the criteria suggested by Gregersen and colleagues
(Gregersen et al., 2007),
namely, (1) positive work should be preceded by negative work (otherwise no
elastic energy could have been stored), (2) the plantarflexor muscles must be
active and exerting force throughout stance [confirmed by a continuous
plantarflexor moment at each joint (Fig.
7) and EMG data (Ishida et
al., 1976; Okada and Kondo,
1982)], and (3) at each joint plantarflexion should not exceed the
amount of dorsiflexion (confirmed by the calculated joint angles;
Fig. 7). Our estimates indicate
that 100% of the positive work performed at the TC joint, and 90% of that
performed at the MT joint could, in theory, come from elastic recoil. We can
therefore conclude that plantarflexor muscle–tendon systems crossing the
TC and TM joints (Achilles' tendon and tendons of the long digital flexors)
can function as springs during hylobatid bipedalism, storing and releasing
elastic energy with each step. Yet, the importance of this recoil for the cost
of bipedal locomotion must be discussed.
To get an idea about the contribution of the positive external work
performed at the foot to whole body propulsion, we compared the power profiles
of the foot joints to those calculated from fluctuations of the centre of mass
(COM) in an earlier publication (Vereecke
et al., 2006b). The positive external work generated at the foot
joints (+0.78 J) amounts to around 54% of the positive external muscular work
(+1.45 J) delivered at COM-level during stance
(Fig. 9) suggesting a
substantial contribution. If we look at the relative timing, however, the foot
joints obviously generate positive power whereas power at COM-level is
negative (Fig. 9), suggesting
that tendon recoil (at foot level) does not contribute to whole-body dynamics.
However, power calculations based on COM fluctuations overlook the work
performed by the individual limbs during double support, as these have an
opposing action. As shown for human walking
(Bastien et al., 2003;
Donelan et al., 2002), the
leading leg performs predominantly negative work, whereas the trailing leg
performs positive work during double support. It seems probable, therefore,
that the positive work output at the level of the foot can still contribute
substantially to countering the braking action of the contralateral (leading)
limb. This is further supported by the observation that the positive work
performed at foot level coincides with the upward movement of the COM (the COM
position is highest during double stance and lowest during midstance; cf.
human running) (Vereecke et al.,
2006b).
In human bipedalism, stretch and recoil of the Achilles' tendon leads to an
energy recovery of 35% (Alexander,
1991b), which is further increased to 52% by flattening of the
longitudinal foot arch and resulting stretching of the extensive plantar
aponeurosis and plantar ligaments (Ker et
al., 1987). Quite unexpectedly, both recovery mechanisms are also
present in gibbon bipedalism. Instead of a flattening of the longitudinal
arch, as seen in human walking and running
(Ker et al., 1987), the flat
and mobile gibbon foot bends during the stance phase [predominantly at the TM
joint, i.e. the so-called `midtarsal break'
(Vereecke et al., 2003;
DeSilva and MacLatchy, 2008)],
potentially storing elastic strain energy in the stretched plantar tendons and
ligaments. Such a `reversed arch' mechanism has previously been described by
Bennett and colleagues in a study on cadaveric feet of monkeys [vervet monkeys
and macaques (Bennett et al.,
1989; Alexander,
1991a)]. They identified the long and short plantar ligament and
the calcaneonavicular/spring ligament as potential sources of elastic energy
storage in the primate foot (see also
Bennett et al., 1989). However,
our results indicate that the relatively strong tendons of the digital flexors
(Vereecke et al., 2005b;
Payne et al., 2006) which run
at the plantar side of the foot, will be even more important energy
stores.
From prehensile tool to efficient lever
In an arboreal setting a flexible foot structure is essential, allowing a
powerful grip in a wide range of locomotor modes and postures (e.g. the
dorsiflexed-supinated foot position in climbing). Considering the arboreal
origin of primates, it is not surprising that most extant nonhuman primates
have flexible feet, and even the foot of humans, obligate terrestrialists,
bears hallmarks of an arboreal ancestry (e.g. the organization of the
intrinsic foot muscles, the variable amount of hallux abductability, and
modified sellar-shape of the talar trochlea)
(Lewis, 1980). In terrestrial
locomotion, however, a flexible foot structure is less favourable than a
`rigid' foot as it has a reduced capacity for generation of propulsion. This
is evident in the force profiles of gibbon bipedalism
(Fig. 6), which lack the sudden
drop of the vertical force at terminal stance associated with a strong
push-off. Such clear propulsive push-off has not been observed in any of the
living apes and seems to be a unique human feature, related to the rigidity of
the human foot in terminal stance (Li et
al., 1996; Crompton et al.,
2008).
The change in foot structure from apes and early hominins to modern humans
is clearly induced by a shift from slow, arboreal to faster, terrestrial
locomotion. The occurrence of pedal modifications associated with terrestrial
cursoriality is certainly not unique to humans; textbook examples include the
specialized foot/hand and limb structure of cursorial mammals. Ungulates (e.g.
horses, giraffes) and carnivores (e.g. wolves, cheetahs) are extreme examples
hereof, characterized by elongated distal limb segments, tarsus and
metatarsus, reduced distal limb mass, joint motion restricted to the
parasagittal plane, and digitigrade or even unguligrade foot/hand posture
(Hildebrand, 1995). Similar
modifications in foot structure and posture have also evolved in the most
committed terrestrial primates: patas monkeys, baboons, geladas (e.g.
elongated legs, long metacarpals/tarsals and relatively short digits, straight
phalanges, digitigrade or semi-plantigrade foot/hand posture, reduced
hallux/pollex) (Ankel-Simons,
1999; Polk, 2002;
Jungers et al., 2005;
Lemelin and Schmitt, 2007) and
humans. According to Bramble and Lieberman
(Bramble and Lieberman, 2004),
nine structures in the human foot can be considered as cursorial adaptations,
including: a stabilized plantar arch, powered and stabilized plantarflexion,
enlarged calcaneal tuberosity, close-packed calcaneocuboid joint, permanently
adducted hallux, short toes and distal mass reduction. Most of these changes
lead to increased stiffness/rigidity and enhanced mechanical leverage of the
human foot, yet without sacrificing its essentially plantigrade and arboreal
configuration which makes it a truly unique structure.
Changes in pedal morphology will only occur if they provide a strong
selective advantage (e.g. improved speed and/or reduced locomotor cost), which
lets us postulate that the specialized modern human foot could only have
evolved in a predominantly terrestrial and cursorial hominin as it provides a
clear benefit in fast terrestrial locomotion yet will compromise arboreal
locomotion (especially fine-branch habitat). However, since the acquisition of
a bipedal gait probably arose in an arboreal setting, and preceded the
adoption of an obligate terrestrial lifestyle, the feet of early hominins
probably remained quite flat and flexible until 4 Ma
(Stern and Susman, 1983;
Harcourt-Smith and Aiello,
2004; Gebo and Schwartz,
2006) and might have displayed a midtarsal break during
bipedalism. Such a midtarsal break, or high midfoot flexibility, is reported
for gibbons, chimpanzees and bonobos
(Bojsen-Møller, 1979;
D'Août et al., 2002;
Vereecke et al., 2003;
Vereecke and Van Sint Jan,
2008; DeSilva and MacLatchy,
2008), and allows the heel to rise while the metatarsals and
phalanges remain on the ground. As shown in this paper, this midfoot
dorsiflexion 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.
To sum up, this study indicates that although a compliant arboreally adapted foot is less mechanically effective for push-off than a `rigid' arched foot, it can contribute to propulsion generation in bipedalism via stretch and recoil of the plantarflexor tendons and plantar ligaments.
LIST OF ABBREVIATIONS
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Acknowledgments |
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
|---|
Alexander, R. M. (1991a). Elastic mechanisms in primate locomotion. Z. Morphol. Anthropol. 78,315 -320.[Medline]
Alexander, R. M. (1991b). Energy-saving
mechanisms in walking and running. J. Exp. Biol.
160, 55-69.
Ankel-Simons, F. (1999). Primate Anatomy: An Introduction. New York: Academic Press.
Bastien, G. J., Heglund, N. C. and Schepens, B.
(2003). The double contact phase in walking children.
J. Exp. Biol. 206,2967
-2978.
Belli, A., Kyrolainen, H. and Komi, P. V. (2002). Moment and power of lower limb joints in running. Int. J. Sports Med. 23,136 -141.[CrossRef][Medline]
Bennett, M. B., Ker, R. F. and Alexander, R. M. (1989). Elastic strain energy storage in the feet of running monkeys. J. Zool. 217,469 -475.
Biewener, A. A. (1983). Allometry of
quadrupedal locomotion: the scaling of duty factor, bone curvature and limb
orientation to body size. J. Exp. Biol.
105,147
-171.
Biewener, A. A. (1998). Muscle–tendon stresses and elastic energy storage during locomotion in the horse. Comp. Biochem. Physiol. B 120, 73-87.[CrossRef][Medline]
Bojsen-Møller, F. (1979).Calcaneocuboid joint and stability of the longitudinal arch of the foot at high and low gear push off. J. Anat. 129,165 -176.[Medline]
Bramble, D. M. and Lieberman, D. L. (2004). Endurance running and the evolution of Homo. Nature 432,345 -352.[CrossRef][Medline]
Cannon, C. H. and Leighton, M. (1994). Comparative locomotor ecology of gibbons and macaques: selection of canopy elements for crossing gaps. Am. J. Phys. Anthropol. 93,505 -524.[CrossRef][Medline]
Carson, M. C., Harrington, M. E., Thompson, N., O'Connor, J. J. and Theologis, T. N. (2001). Kinematic analysis of a multi-segment foot model for research and clinical applications: a repeatability analysis. J. Biomech. 34,1299 -1307.[CrossRef][Medline]
Clarke, R. J. (2003). Bipedalism and arboreality in Australopithecus. Cour. Forsch.-Inst. Senckenberg 243,79 -83.
Crompton, R. H., Vereecke, E. E. and Thorpe, S. K. S. (2008). Locomotion and posture from the common hominoid ancestor to fully modern hominins, with special reference to the last common panin/hominin ancestor. J. Anat. 212,501 -543.[CrossRef][Medline]
D'Août, K., Aerts, P., De Clercq, D., De Meester, K. and Van Elsacker, L. (2002). Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus). Am. J. Phys. Anthropol. 119, 37-51.[CrossRef][Medline]
DeSilva, J. M. and MacLatchy, L. M. (2008). Revisiting the midtarsal break. Am. J. Phys. Anthropol. 135,S46; 89.
Donatelli, R. A. (1996). The Biomechanics of the Foot and Ankle. 2nd edn. Philadelphia: F.A. Davies.
Donelan, J. M., Kram, R. and Kuo, A. D. (2002).
Mechanical work for step-to-step transitions is a major determinant of the
metabolic cost of human walking. J. Exp. Biol.
205,3717
-3727.
Filler, A. (2007). Homeotic evolution in the Mammalia: diversification of Therian axial seriation and the morphogenetic basis of human origins. PLoS ONE 2, e1019.[CrossRef]
Fleagle, J. G. (1976). Locomotion and posture of the Malayan siamang and implications for hominid evolution. Folia Primatol. 26,245 -269.[CrossRef][Medline]
Fleagle, J. G. (1999). Primate Adaptation and Evolution. 2nd edn. New York: Academic Press.
Fuller, E. A. (2000). The windlass mechanism of the foot-a mechanical model to explain pathology. J. Am. Podiatr. Med. Assoc. 90,35 -46.[Abstract]
Gebo, D. L. (1993). Functional morphology of the foot in primates. In Postcranial Adaptation in Nonhuman Primates (ed. D. L. Gebo). DeKalb: Northern Illinois University Press.
Gebo, D. L. and Schwartz, G. T. (2006). Foot bones from Omo: implications for hominid evolution. Am. J. Phys. Anthropol. 129,499 -511.[CrossRef][Medline]
Gershman, S. (1988). A literature review of midtarsal joint function. Clin. Podiatr. Med. Surg. 5, 385-391.[Medline]
Gittins, P. S. (1983). Use of forest canopy by the agile gibbon. Folia Primatol. 40,134 -144.[CrossRef][Medline]
Gregersen, C. S., Silverton, N. A. and Carrier, D. R. (2007). External work and potential for elastic energy storage at the limb joint of running dogs. J. Exp. Biol. 201,3197 -3210.
Hansen, A. H., Childress, D. S., Miff, S. C., Gard, S. A. and Mesplay, K. P. (2004). The human ankle during walking: implications for design of biomimetic ankle prostheses. J. Biomech. 37,1467 -1474.[CrossRef][Medline]
Harcourt-Smith, W. E. H. and Aiello, L. C. (2004). Fossils, feet and the evolution of human bipedal locomotion. J. Anat. 204,403 -416.[CrossRef][Medline]
Harrison, T. and Rook, L. (1997). Enigmatic anthropoid or misunderstood ape? The phylogenetic status of Oreopithecus bambolii reconsidered. In Function, Phylogeny, and Fossils: Miocene Hominoid Evolution and Adaptations (ed. D. R. Begun, C. V. Ward and M. D. Rose), pp. 327-362. New York: Plenum Press.
Hicks, J. H. (1954). The mechanics of the foot: II. the plantar aponeurosis and the arch. J. Anat. 88, 25-30.[Medline]
Hildebrand, M. (1995). Analysis of Vertebrate Structure. 4th edn. New York: Wiley.
Ishida, H., Kimura, T., Okada, M. and Yamazaki, N. (1976). Kinesiological aspects of bipedal walking in gibbons. Gibbon Siamang 4,135 -145.
Jungers, W. L., Lemelin, P., Godfrey, L. R., Wunderlich, R. E., Burney, D. A., Simons, E. L., Chatrath, P. S., James, H. F. and Randria, G. F. (2005). The hands and feet of Archaeolemur: metrical affinities and their functional significance. J. Hum. Evol. 49,1 , 36-55.[CrossRef][Medline]
Ker, R. F., Bennett, M. B., Bibby, R. S., Kester, R. C. and Alexander, R. M. (1987). The spring in the arch of the human foot. Nature 325,147 -149.[CrossRef][Medline]
Kidd, R. S., O'Higgins, P. and Oxnard, C. E. (1996). The OH8 foot: a reappraisal of the hindfoot utilizing a multivariate analysis. J. Hum. Evol. 31,269 -291.[CrossRef]
Kidder, S. M., Abuzzahab, F. S. J., Harris, G. F. and Johnson, J. E. (1996). A system for the analysis of foot and ankle kinematics during gait. IEEE Trans. Rehabil. Eng. 4, 25-32.[CrossRef][Medline]
Klenerman, L. and Wood, B. (2006). The Human Foot: A Companion to Clinical Studies. Heidelberg: Springer.
Kwon, Y.-H. (1994). Kwon 3D Motion Analysis Package 2.1, User's reference manual. V-TEK Corporation. Korea: Anyang.
Lemelin, P. and Schmitt, D. (2007). Origins of grasping and locomotor adaptations in primates: comparative and experimental approaches using an opossum model. In Primate Origins: Adaptations and Evolution (ed. M. J. Ravosa and M. Dagosto), pp.329 -380. New York: Springer.
Lewis, O. J. (1980). The joints of the evolving foot: part 1, the ankle joint. J. Anat. 130,527 -543.[Medline]
Li, Y., Crompton, R. H., Alexander, R. M., Gunther, M. M. and Wang, W. J. (1996). Characteristics of ground reaction forces in normal and chimpanzee-like bipedal walking by humans. Folia Primatol. 66,137 -159.[CrossRef][Medline]
MacWilliams, B. A., Cowley, M. and Nicholson, D. E. (2003). Foot kinematics and kinetics during adolescent gait. Gait Posture 17,214 -224.[Medline]
Madar, S. I., Rose, M. D., Kelley, J., MacLatchy, L., Pilbeam, D. (2002). New Sivapithecus postcranial specimens from the Siwaliks of Pakistan. J. Hum. Evol. 42,705 -752.[CrossRef][Medline]
Okada, M. and Kondo, S. (1982). Gait and EMG during bipedal walk of a gibbon (Hylobates agilis) on flat surface. J. Anthrop. Soc. Nippon 90, 3,325 -330.
Payne, R. C., Crompton, R. H., Günther, M. M., D'Août, K., Savage, R., Isler, K. and Vereecke, E. (2006). Morphological analysis of the hindlimb in apes and humans. Part I: Muscle Architecture. J. Anat. 208,709 -724.[CrossRef][Medline]
Pickford, M. (2006). Paleoenvironments, paleoecology, adaptations and the origins of bipedalism in Hominidae. In Human Origins and Environmental Backgrounds (ed. H. Ishida, R. H. Tuttle, M. Pickford, M. Ogihara and M. Nakatsukasa), pp.175 -198. Heidelberg: Springer.
Pickford, M., Senut, B., Gommery, D. and Treil, J. (2002). Bipedalism in Orrorin tugenensis revealed by its femora. C. R. Palevol. 1, 191-203.[CrossRef]
Polk, J. D. (2002). Adaptive and phylogenetic
influences on musculoskeletal design in cercopithecine primates. J.
Exp. Biol. 205,3399
-3412.
Prost, J. H. (1980). Origin of bipedalism. Am. J. Phys. Anthropol. 52,175 -198.[CrossRef][Medline]
Richmond, B. G. and Jungers, W. L. (2008).
Orrorin tunegensis femoral morphology and the evolution of hominin
bipedalism. Science 319,1662
-1665.
Sati, J. P. and Alfred, J. R. B. (2002). Locomotion and posture in Hoolock gibbon. Ann. For. 10,298 -306.
Schmitt, D. and Larson, S. G. (1995). Heel contact as a function of substrate type and speed in primates. Am. J. Phys. Anthropol. 96,39 -50.[CrossRef][Medline]
Senut, B. (2003). Palaeontological approach to the evolution of hominid bipedalism: the evidence revisited. Cour. Forsch.-Inst. Senkenberg 243,125 -134.
Senut, B. (2006). Arboreal origins of bipedalism. In Human Origins and Environmental Backgrounds (ed. H. Ishida, R. H. Tuttle, M. Pickford, N. Ogihara and M. Nakatsukasa), pp. 199-208. Heidelberg: Springer.
Simonsen, E. D., Dyhre-Poulsen, P., Voigt, M., Aagaard, P. and Falletin, N. (1997). Mechanisms contributing to different joint moments observed during human walking. Scand. J. Med. Sci. Sports 7,1 -13.[Medline]
Stern, J. T. (1975). Before bipedality. Yearb. Phys. Anthropol. 19, 59-68.
Stern, J. T. and Susman, R. L. (1983). The locomotor anatomy of Australopithecus afarensis. Am. J. Phys. Anthropol. 60,279 -317.[CrossRef][Medline]
Thorpe, S. K. S., Holder, R. L. and Crompton, R. H.
(2007). Origin of human bipedalism as an adaptation for
locomotion on flexible branches. Science
316,1328
-1331.
Tuttle, R. H. (1969). Knuckle-walking and the evolution of Hominoid hands. Am. J. Phys. Anthropol. 26,171 -206.
Tuttle, R. H. (1981). Evolution of hominid
bipedalism and prehensile capabilities. Philos. Trans. R. Soc.
Lond., B, Biol. Sci. 292,89
-94.
Vaughan, C. L. (1996). Are joint torques the Holy Grail of human gait analysis? Hum. Mov. Sci. 15,423 -443.[CrossRef]
Vereecke, E. E., D'Août, K., De Clercq, D., Van Elsacker, L. and Aerts, P. (2003). Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus). Am. J. Phys. Anthropol. 120,373 -383.[CrossRef][Medline]
Vereecke, E. E., D'Août, K., De Clercq, D., Van Elsacker, L. and Aerts, P. (2005a). Functional analysis of the gibbon foot during terrestrial bipedal walking: plantar pressure distributions and 3D ground reaction forces. Am. J. Phys. Anthropol. 128,659 -669.[CrossRef][Medline]
Vereecke, E. E., D'Août, K., Payne, R. and Aerts, P. (2005b). Functional analysis of the foot and ankle myology of gibbons and bonobos J. Anat. 206,453 -476.[CrossRef][Medline]
Vereecke, E. E., D'Août, K. and Aerts, P. (2006a). Speed modulation in hylobatid bipedalism: a kinematical analysis. J. Hum. Evol. 51,513 -526.[CrossRef][Medline]
Vereecke, E. E., D'Août, K. and Aerts, P.
(2006b). The dynamics of hylobatid bipedalism: evidence for an
energy-saving mechanism? J. Exp. Biol.
209,2829
-2838.
Vereecke, E. E. and Van Sint Jan, S. (2008). The functional anatomy of the ape foot. In Advances in Plantar Pressure Measurements in Clinical and Scientific Research (ed. K. D'Août, K. Lescrenier and B. Van Gheluwe), pp.89 -106. Maastricht: Shaker Publishing BV.
Wells, R. P. (1981). The projection of ground reaction force as a predictor of internal joint moments. Bull. Prosthet. Res. 18,15 -19.
Winter, D. A. (1990). The Biomechanics and Motor Control of Human Movement. 3rd edn. New York: Wiley.
Wolde Gabriel, G., Haile-Selassie, Y., Renne, P. R., Hart, W. K., Ambrose, S. H., Asfaw, B., Heiken, G. and Witte, T. (2001). Geology and palaeontology of the Late Miocene Middle Awash valley, Afar rift, Ethiopia. Nature 412,175 -178.[CrossRef][Medline]
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