J. Anat. (2004) 204, pp353–361
REVIEW
Blackwell Publishing, Ltd.
Locomotion in bonobos (Pan paniscus): differences and
similarities between bipedal and quadrupedal terrestrial
walking, and a comparison with other locomotor modes
K. D’Août,1,2 E. Vereecke,1,2 K. Schoonaert,1,2 D. De Clercq,3 L. Van Elsacker2 and P. Aerts1
1
Department of Biology, University of Antwerp, Belgium
Centre for Research and Conservation, Royal Zoological Society of Antwerp, Belgium
3
Movement and Sport Sciences, Ghent University, Belgium
2
Abstract
One of the great ongoing debates in palaeo-anthropology is when, and how, hominids acquired habitual bipedal
locomotion. The newly adopted bipedal gait and the ancestral quadrupedal gait are most often considered as very
distinct, with each habitual locomotor mode showing corresponding anatomical adaptations. Bonobos (Pan paniscus),
along with common chimpanzees (P. troglodytes), are the closest living relatives to humans and their locomotion
is valuable for comparison with other primates, and to gain an insight in the acquisition of human bipedalism.
Bonobos are habitual quadrupeds, but they also engage in bipedal locomotion, both on terrestrial and in arboreal
substrates. In terms of kinematics and dynamics, the contrast between bipedal and quadrupedal walking seems
to be more subtle than one might expect. Apart from the trunk being approximately 37 ° more erect during
bipedal locomotion, the leg movements are rather similar. Apart from the heel, plantar pressure distributions
show subtle differences between bipedal and quadrupedal locomotion. Regardless, variability is high, and various
intermediate forms of locomotion (e.g. tripedal walking) exist both in captivity and in the wild. Moreover, there is
overlap between the characteristics of walking and other locomotor modes, as we show with new data of walking
on an inclined pole and of vertical squat jumps. We suggest that there is great overlap between the many locomotor
modes in bonobos, and that the required polyvalence is reflected in their anatomy. This may hamper the
development of one highly specialized gait (i.e. bipedalism), which would constrain performance of the other types
of locomotion.
Key words bipedalism; bonobos; kinematics; kinetics; pan paniscus; primate locomotion; quadrupedalism.
Introduction
The acquisition of habitual bipedalism is considered
as the most prominent milestone in hominid evolution,
and it is used as a hominid identifying mark (see, e.g.
Boyd & Silk, 2000). However, it is not trivial to determine
the locomotor mode of (pre)hominids because of the
lack of (mostly postcranial) remains and, even if they
are present, the interpretation of anatomical features.
Correspondence
Dr Kristiaan D’Août, Department of Biology, University of Antwerp,
Campus Drie Eiken, Universiteitsplein 1, B-2610 Antwerpen, Belgium.
T: +32 (0)3 820.22.69; F: +32 (0)3 820.22.71; E: [email protected]
Accepted for publication 9 March 2004
© Anatomical Society of Great Britain and Ireland 2004
Very little direct evidence for the gait of extinct
hominids is available (exceptions include the Laetoli
footprints; Leakey & Hay, 1979) and therefore analogy
with extant species proves essential. Modern humans
differ drastically from the early hominids that may have
acquired habitual bipedalism (see, e.g. Zihlman, 1984) and
therefore the great apes, closest related to hominids
(Benton, 1997), and for which both anatomy and gait
can be studied, may provide crucial information.
All great apes (and some other primates) have been
proposed as models for early hominids, often for different
reasons. From a phylogenetic point of view, chimpanzees
(Pan troglodytes) and bonobos (P. paniscus) are the
most obvious species because they are related most
closely to humans, and recently it has even been proposed
354 Bipedal and quadrupedal terrestrial walking, K. D’Août et al.
that they should be placed within the genus Homo
(Wildman et al. 2003).
Of these two species, based on postcranial anatomy
and evolutionary history, bonobos are considered to
provide the best model, although chimpanzees might
be alternative candidates as well (Corruccini & McHenry,
1979). By contrast, orang-utans (Pongo pygmaeus), more
distantly related to the hominids (Benton, 1997), show
interesting features in their locomotion repertoire that
may also have been part of the prehominid’s repertoire as well and may therefore also be particularly
fruitful study subjects (Crompton et al. 2003). Gorillas
(Gorilla gorilla) engage in bipedal postures (for display
rather than locomotion) more than other apes and may
therefore show more adaptations towards bipedalism
and, consequently, be relevant study species.
It is clear that no living species is a perfect model or
stand-in for the hominid that first acquired habitual
bipedalism (assuming that this species could be known).
Therefore, a comparative approach studying as many
relevant species as possible should be used to shed light
on the likelihood of existing hypotheses bearing on
the acquisition of habitual bipedalism in hominids, and
reveal general principles of hominoid locomotion that
are likely to have existed in early hominids as well (see
Schmitt, 2003, for an overview).
This paper presents a non-exhaustive review of the
experimental data known to date on bonobo locomotion,
focusing primarily on bipedal walking. Based on the
available data (taken from the literature and from
unpublished results), we evaluate how bipedal locomotion fits in with the bonobo’s overall locomotor repertoire, compare to what extent kinesiological parameters
differ between bipedal walking and other locomotor
modes, and discuss some implications towards studies
of bipedal locomotion in apes and hominids.
Bipedal vs. quadrupedal terrestrial walking
Spatiotemporal gait characteristics
When bonobos walk quadupedally, they typically use a
diagonal-sequence walking gait, like other primates,
but unlike most quadrupeds, who typically use a lateralsequence walk (Hildebrand, 1967; see Larson, 1998, for
details). At high velocities, bonobos will gallop; we have
never observed a trot, which may be an unfavourable
gait because such a high-stiffness, high-frequency gait
would lead to excessively high peak stresses on the
limbs (Schmitt, 1995 in Larson, 1998; Schmitt, 1999) or
would not allow for an efficient recovery stroke in animals
with distally heavy limbs (and resulting high moments
of inertia about the hip) (Preuschoft & Günther, 1994;
Preuschoft et al. 1996). Quantitative data on galloping
bonobos are lacking in the literature.
Aerts et al. (2000) compared spatiotemporal gait characteristics between bipedally and quadrupedally walking
bonobos (Fig. 1). The duty factor (the fraction of the time
for which each foot is on the ground) is similar in both
gaits, but the relationship between walking velocity and
stride frequency (and hence stride length and step length)
differs. In any gait, bonobos increase velocity by increasing
both the stride length and the stride frequency, but the
slope of these paramaters differs, both when absolute
values are used or when the data are made dimensionless using the principle of dynamic similarity (see
Alexander, 2004). For a given velocity, bonobos walking
bipedally will use shorter steps and strides but a higher
stride frequency than when walking quadrupedally.
Segment and joint angles
Bonobos typically display a bent-hip, bent-knee posture
during bipedal locomotion but also during quadrupedal
Fig. 1 Gait parameters during bipedal and quadrupedal walking in bonobos (after Aerts et al. 2000). Dimensionless values are
presented (see Aerts et al. 2000, for details), with a stride being a full gait cycle. For clarity, only the regression lines through the
actual data points are shown.
© Anatomical Society of Great Britain and Ireland 2004
Bipedal and quadrupedal terrestrial walking, K. D’Août et al. 355
Fig. 2 Joint angles during bipedal and quadrupedal walking in bonobos (after D’Août et al. 2002). The angles are defined as the
enclosed angle in the sagittal plane between the segments that form the considered joint (i.e. full flexion = 0°, full
extension = 180°). The foot is modelled as one segment from the posteroventral edge of the heel bone to the distalmost toe.
Fig. 3 Example vertical ground-reaction force
profiles from a bonobo walking bipedally (A), a
bonobo walking quadrupedally (B), a bonobo
walking over a 30° inclined pole (C) (K. Schoonaert
et al., unpublished data) and a human (D, after
Farley & Ferris, 1998). For comparison, all forces are
scaled to 100% peak force.
locomotion. D’Août et al. (2002) quantified the hip,
knee and ankle angle throughout the stride for both
gait types. Time plots of these joint angles have similar
shapes (Fig. 2). During the greater part of stance phase,
the hip extends, but it may already begin to flex at the
end of stance phase, when the heel is lifted but the
forefoot remains in contact with the ground. The knee
flexes considerably throughout stance, most importantly at initial contact and shortly before swing phase.
The foot is placed quite flat on to the substrate in
bonobos (see below), and thus the ankle first flexes and
then extends during stance, but the latter not as fast as
during the human push-off. In general, remarkably few
significant differences were found between the angle
values of bipedal and quadrupedal walking at selected
phases of the stride. On average, the trunk is held 37°
more erect during bipedal walking than during quadrupedal walking. Consequently, the hip angle is larger
(i.e. more extended) throughout the stride (Fig. 2).
Selected angle values of the thigh, shank and foot,
and the resulting knee and ankle angles, do not differ
© Anatomical Society of Great Britain and Ireland 2004
significantly between bipedal and quadrupedal walking
(D’Août et al. 2002).
Kinetics
Figure 3 shows sample vertical ground reaction forces
of bonobos (Schoonaert et al. 2003). Although variability
appears to be higher than in human walking, it is consistently single-humped. A double-humped profile, as
seen for human walking (but not running), is not observed,
but a sharp peak corresponding with heel impact is
frequently observed. From this, we conclude that bonobos
do not use an ‘inverted pendulum’-type gait, as further
confirmed by the very low vertical oscillations of the
body’s centre of mass during both bipedal and quadrupedal walking (D’Août et al. 2001; Schoonaert et al. 2003).
Pedobarography
Vereecke et al. (2003) compared plantar pressures for
bipedally and quadrupedally walking bonobos (Fig. 4).
356 Bipedal and quadrupedal terrestrial walking, K. D’Août et al.
the substrate first) back to the heel region and then
forwards. Quantitative analyses of selected zones under
the foot indicate a clear difference in peak pressures
under the heel, which is much higher in quadrupedal
than in bipedal walking. However, relative impulses
of all selected zones under the foot (including the heel)
are not significantly different between both gait types,
and load is carried by the whole foot throughout almost
the whole stance phase.
Gait asymmetry
Fig. 4 Time course of plantar pressure under selected zones of
the bonobo foot while walking bipedally and quadrupedally
(data from Vereecke et al. 2003). All profiles are normalized to
100% contact time.
The general foot roll-off pattern, shown by the path and
time course of the centre of pressure (COP) under the
feet, is very variable during both bipedal and quadrupedal bouts. In most cases, initial contact is made
almost simultaneously by the heel and the lateral midfoot. The COP then travels forward, typically following
a curved course along the lateral rays and moving
medially at the end of stance. Alternative patterns may
vary from an almost straight COP course from the heel
to the second digit, to a V-curved course in which the
COP travels from the hallux (which may occasionally hit
It has already been established that quadrupedally
walking primates often ‘overstride’, placing their
feet in front of the ipsilateral hand (for an overview,
see Larson, 1998). This allows them to use long strides
and correspondingly low stride frequencies for a given
velocity, which in turn may reduce internal work (Raichlen,
2003). Furthermore, and unlike most other mammals,
primates typically use a diagonal sequence/diagonal
couplets quadrupedal walk, in which diagonal limbs move
as a pair (Hildebrand, 1967). Both of these features are
typically (but not always) found in bonobo quadrupedal
sequences. As in other primates, an overstriding foot
may be placed medially of the ipsilateral hand (‘inside
foot’) or laterally of the ipsilateral hand (‘outside
foot’), and this possibly has an important effect as to
the spatial (a)symmetry of the gait.
We have analysed quadrupedal walks of bonobos,
focusing on left–right differences of the walk. Preliminary data (D’Août et al. 2003) strongly suggest that
individuals use both (‘inside’ and ‘outside’) foot placements, but that they have an individual preference for
one type. Furthermore, an ‘inside’ foot, being placed
more medially and thus closer to the vertical projection
of the body’s centre of mass, can be expected to carry
more load than an ‘outside’ foot. Our tentative data for
six quadrupedal sequences (of one adult female and two
adult males) confirm this and, moreover, show higher
vertical ground reaction peak forces for the ‘inside’ foot.
Plantar pressure recordings suggest a flatter placement
of ‘inside’ feet than ‘outside’ feet, with a more laterally
travelling centre of pressure and a more abducted hallux.
The way in which the foot is placed during quadrupedal
walking also influences the orientation of the body
with respect to the overall direction of progression:
the body will be positioned obliquely, e.g. when the
left foot is ‘inside’, the longitudinal body axis will be
shifted (the animal will ‘look’) to the right.
© Anatomical Society of Great Britain and Ireland 2004
Bipedal and quadrupedal terrestrial walking, K. D’Août et al. 357
We found that the oblique positioning of the trunk
is not only typical for quadrupedal walking, but also
for bipedal walking and that here, too, some kinesiological left /right differences are found in our bipedal
sequences. For instance, when the body is rotated to
the left with respect to the walking direction, the right
foot will be ‘leading’ and the left foot may strike not
much anteriorly of the right foot, staying closely under
the body’s centre of mass. In this respect, the ‘leading’
foot may be functionally comparable with an ‘outside’
foot during quadrupedal walk, and the ‘trailing’ foot
to the ‘inside’ foot, carrying more load.
Although our preliminary data clearly suggest that
left /right differences in foot function are systematic
and that they are similar for bipedal and quadrupedal
bouts, more quantitative data are clearly required.
They are not trivial to collect because, as variability in
bonobo gait is high, study sequences should ideally
consist of at least two consecutive strides of a single
walking sequence, each with documented groundreaction forces and plantar pressure data.
Terrestrial walking vs. other locomotor modes
Terrestrial locomotion
Although research on terrestrially walking bonobos
(and other apes) has typically contrasted bipedal with
quadrupedal locomotion, and indeed found differences
(see above), it should be stressed that the discrete
subdivision between both gait types may only reflect
extremes in a continuous range of terrestrial walking
styles, in which different walking styles fade into each
other. Figure 5 illustrates this point by showing
some locomotor postures during untrained walking of
bonobos. Typical quadrupedal and bipedal postures
are shown in panels 1 and 5, respectively. Panels 2–4
illustrate alternative locomotor modes. In a range from
typical knuckle walking to bipedal walking, we may
observe tripedal walking (panel 2), very crouched
bipedal walking with an occasional hand–ground
contact (panel 3) and crouched bipedal walking
(panel 4). Intermediate locomotor modes are observed
less frequently than the typical extremes, but are not
anomalous. For example, Susman (1984) and Kano (1992)
describe tripedal locomotion in wild bonobos, and
it has also been observed in chimpanzees (Kelly, 2001).
This overview is not exhaustive, but illustrates that the
clear-cut subdivision between bipedal and quadrupedal
walking in apes may be somewhat artificial. Although
quantitative data are lacking for the intermediate
gaits, we presume gait parameters may change in a
continuous fashion.
Observations on bipedal walking and terrestrial
locomotion in the wild and in captivity
Bipedal walking and other terrestrial locomotion types
in wild bonobos have been described in three sites
in the Democratic Republic of Congo. The observations
suggest that the locomotor types, as found in captivity,
reflect natural behaviour. In Wamba, a wet and densely
forested site but with sugarcane fields to facilitate
observations, apart from arboreal locomotion such as
brachiation and climbing, the habituated bonobos
engage in several forms of terrestrial locomotion:
either quadrupedalism (knuckle walking), bipedalism
(sometimes over a distance of 20 m or more), as well as
tripedal walking (Kano, 1992). In Lomako, which is also
wet and densely forested, terrestrial locomotion also
included bipedal walking (Susman et al. 1980) and
tripedal walking (Susman, 1984; Doran, 1993). Recent
observations from Lukuru, a dry forest/savanna mosaic
habitat, report frequent bipedal walking through
Fig. 5 Example body postures during terrestrial walking. Note that there is a continuum from left to right, with A being a typical
quadrupedal ‘knuckle-walking’ posture and E a typical bipedal ‘bent-hip, bent-knee’ posture. B illustrates tripedal walking.
© Anatomical Society of Great Britain and Ireland 2004
358 Bipedal and quadrupedal terrestrial walking, K. D’Août et al.
Fig. 6 Hip angle during during terrestrial bipedal and
guadrupedal walking, climbing on a 30° inclined pole, vertical
climbing (after Isler, 2003) and vertical jumping (M. Scholz
et al., unpublished data). Definition of angles as in Fig. 2. The
jumping curve is an average of five high sequences of one
individual, and the plot goes from maximal flexion
(corresponding well with the start of jumping) to toe-off.
Fig. 7 Knee angle during during terrestrial bipedal and
guadrupedal walking, climbing on a 30° inclined pole, vertical
climbing (after Isler, 2003) and vertical jumping (M. Scholz
et al., unpublished data). Definition of angles as in Fig. 2. The
jumping curve is an average of five high sequences of one
individual, and the plot goes from maximal flexion
(corresponding well with the start of jumping) to toe-off.
open short-grass plains, along roadsides and in shallow
pools (Thompson, 2002).
In the wild, unaided, bipedal walking bouts represent
as low as 0.3% of terrestrial travel (Doran, 1993), but
bipedalism apparently decreased when habituation
increased (Susman, 1984; Doran, 1993), so it may be
more frequent than direct observations in the wild
suggest.
Observations of captive bonobo populations vary
widely. Unsupported bipedal locomotion may occupy
less than 0.01% of the total time budget (calculated from
Dielentheis et al. 1996). In our work on the population
of the Wild Animal Park of Planckendael (Belgium),
high frequencies of bipedal walking (as a percentage
of bipedal plus quadrupedal locomotion bouts) were
found, ranging from 3.9% for spontaneous bouts to
18.9% when abundant food is supplied (Duchêne,
1997; see also Videan & McGrew, 2001, 2002).
during bipedal walking than during climbing. Isler (2002)
describes that bonobo climbing is more versatile than,
for instance, gorilla climbing.
Vertical jumping
Jumping is a specific type of locomotion in which bonobos
frequently engage both in arboreal and in terrestrial
settings (our personal observations). During vertical
jumping, bonobos will start from a deeply crouched
resting position in which the hip is considerably more
flexed (i.e. to a joint angle of approximately 20°) than
during any other gait type studied. At the end of the
push-off phase, the hip is even slightly more extended
than in bipedal walking (Fig. 6). A similar pattern holds
true for the knee and thus, for both joints, the range of
motion of vertical jumping encompasses completely
that of all other locomotor types studied.
Arboreal locomotion
Locomotion and anatomy
Isler (2002, 2003) examined the kinematics of vertical
climbing along a rope in bonobos, and Schoonaert
et al. (2003) studied climbing on an instrumented pole
with a slope of 30°. Joint angle curves, compared with
terrestrial locomotion, are shown in Figs 6 and 7. In
general, climbing on a 30° inclined pole shows more
resemblance to quadrupedal terrestrial locomotion
than to bipedal locomotion (Lauwers, 2003). This appears
not to hold true for vertical climbing (Isler, 2002). Thus
far, all studies indicate that hip extension is larger
It has been long established that the overall morphology
of P. paniscus is generalized, more so than for the
common chimpanzee (Coolidge, 1933). Data on limb
length and weight distribution and tissue composition
(Zihlman, 1984) confirm this, and suggest that from a
morphological point of view, P. paniscus most closely
resembles the common Pan –hominid ancestor.
More detailed anatomy and morphometry of the
locomotor apparatus has been carried out recently
(Payne & Crompton, 2001; Payne, 2001), and helps
© Anatomical Society of Great Britain and Ireland 2004
Bipedal and quadrupedal terrestrial walking, K. D’Août et al. 359
explain anatomical adaptations towards locomotion.
Compared with the habitually bipedal modern humans,
bonobo anatomy was found to be more generalistic
and indicative of an arboreal lifestyle. The relatively
small moment arms about the hindlimb joints, along
with relatively long fascicles, show that mobility is
favoured at the expense of tension production. Among
African apes, the bonobo resembles modern humans
better in this respect (Payne, 2001), but less so than
the highly arboreal orang-utan (Pongo pygmaeus), so
this characteristic is not necessarily an adaptation for
bipedalism per se.
Discussion and conclusions
Bipedal locomotion in bonobos is highly variable and in
many kinesiological characteristics significant differences
from quadrupedal walking and from other locomotor
modes are found.
Should this lead to the conclusion that bonobo bipedal
locomotion is an exceptional gait type with unique
features? In fact, two major arguments challenge
this statement, as outlined below.
First, the differences between gait characteristics
of bipedal locomotion and other gaits are often more
subtle than one might expect (and drastically different
from walking in modern humans). For example, the
angular displacements of leg joint and segments are
remarkably similar and the differences that are found
(most importantly, the greater hip extension) can be
attributed to the more erect position of the trunk
during typical bipedal locomotion (D’Août et al. 2002).
However, even greater hip extension is found during
jumping.
Pedobarographic records show overlap between
bipedal and quadrupedal walking, and the only striking difference is the higher impact of the heel during
quadrupedal locomotion. Other differences, if present,
are quite subtle and, in general, foot roll-off during both
gait types follows similar (albeit variable) patterns
(see Vereecke et al. 2003).
Secondly, and importantly, although bipedalism is
easily defined as a locomotor mode in which only the
hindlimbs interact with the substrate, this may be
an oversimplification. Ou personal observations under
seminatural circumstances (see Fig. 5) demonstrate that
bipedal sequences cover a range from ‘typical’ bipedal
bouts to very crouched bouts. Although quantitative
data on such sequences are lacking, it is likely that their
© Anatomical Society of Great Britain and Ireland 2004
characteristics would be different and may be closer to
(or overlapping with) other locomotor modes. As such,
different locomotor modes blend into each other to
form a continuum. Interestingly, various forms of
terrestrial locomotion, including tripedal locomotion as an
intermediate form between bipedal and quadrupedal
locomotion, are observed quite regularly in captivity
but also in the wild.
The variability both within and between gait types
in bonobos correpsonds well with anatomical findings.
Apes in general, and bonobos in particular, show
anatomical features that favour manoeuvrability and
versatility (see above).
Clearly, more data are required. Specifically, we
need (1) a more profound insight into ape locomotion
including as much non-invasive methods as possible
(e.g. inverse dynamics), (2) quantitative data of more
locomotor modes (e.g. climbing at different angles
and brachiation) in a wide range of hominoid species
and (3) a better knowledge of locomotor behaviour and
kinesiology in the wild.
So, although our understanding of bonobo or ape
locomotion is far from complete, what can the available
data reviewed here tell us regarding bipedalism in this
species and more generally about apes and possibly
hominids?
Because of the variability of bipedalism, its overlap
with other locomotor modes and the associated polyvalent anatomy, we suggest that the ability for terrestrial bipedalism may be a mere ‘free bonus’ locomotor
mode and, in other words, unspecialized, bonobo- or
ape-like terrestrial bipedalism may not be that difficult
to accomplish. In this respect, recent data confirm
statements made by Zihlman (1984): ‘Given the morphology and behavioral abilities of pygmy chimpanzees,
it is no longer necessary to hypothesize an unusual gait
in order to characterize the locomotor pattern of early
hominids’, and that: ‘The possible existence of an ape
ancestor like P. paniscus suggests no great morphological
leap from the quadrupedal ape ancestor to hominids,
and perhaps less of a behavioral leap than previously
thought’, as well as Isler’s view that: ‘In a hypothetical
light-weighted ancestral hominoid, a corresponding
flexibility could have opened ways to new locomotor
behaviours such as frequent or habitual bipedalism’
(Isler, 2003).
Terrestrial bipedalism in bonobos (or bent-hip, bentknee locomotion in general) is clearly not as specialized
and efficient as in modern humans (see, e.g. Crompton
360 Bipedal and quadrupedal terrestrial walking, K. D’Août et al.
et al. 1998). It is likely that such specialization would
constrain other, more frequently used, locomotor modes,
such as the various arboreal locomotor styles.
Although frequencies of natural bipedal locomotion
are low, injured bonobos are capable of sustained
bipedal locomotion (Van Lawick-Goodall, 1968; Bauer,
1977, in Zihlman, 1984) and it was recently found in a
wild population of common chimpanzees that they
also may engage in bipedalism very frequently under
certain ecological conditions (Stanford, 2002). Generalizing
the bonobo findings to palaeo-anthropological interpretations, we suggest that care should be taken when
assessing locomotor abilities realting to fossil findings:
even if clear adaptations for bipedalism are absent,
bipedalism may have been a significant (but probably
not habitual) part of their locomotion repertoire.
Acknowledgements
We wish to thank the bonobo keepers, the technicians
and the staff of the Wild Animal Park of Planckendael
for help with setting-up the experiments. This work
was funded by the Fund for Scientific ResearchFlanders (FWO-Vl, project G.020999) and by the Flemish
Government through structural support of the Centre
for Research and Conservation (CRC). E.V. and K.S. are
supported by the FWO-Vl and by the CRC, respectively.
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