Studying bonobo (Pan paniscus) locomotion using an integrated

Primatologie, 2001, 4, 191-206
Studying bonobo (Pan paniscus) locomotion
using an integrated setup in a zoo
environment: preliminary results
Kristiaan D'Août1, Peter Aerts1,
Dirk De Clercq2, Kirsten Schoonaert1, Evie Vereecke1,
and Linda Van Elsacker1,3
1. Department of Biology, University of Antwerp, Belgium
2. Movement and Sport Sciences, University of Ghent, Belgium
3. Centre for Research and Conservation, KMDA, Belgium
Abstract
We describe a setup, in the Animal Park of Planckendael (Belgium), for an
integrated study of terrestrial locomotion in bonobos (Pan paniscus). The
setup consists of two orthogonal video cameras (50 Hz), and of three
synchronized measurement units (250 Hz) incorporated in the floor of the
walkway. Each unit consists of a force plate and a functionally coupled highresolution pressure-sensitive mat. Preliminary results show that terres-trial
locomotion in bonobos is very variable. Stride length and stride fre-quency
during bipedal and quadrupedal walking on the setup do not differ
significantly from previously gathered data under semi-natural conditions. As
an example, we present kinematic, force and plantar pressure data of one
bipedal and one quadrupedal sequence. In these preliminary analyses,
displacements of the center of mass are limited in the vertical direction. In
both cases, the animals adopted "bent-hip, bent-knee" postures throughout
the gait cycle. As for the kinematic measures, vertical ground-reaction forces
are variable. A clear double-humped profile (as seen in the human "invertedpendulum" type locomotion) is not observed. Plantar pressure
__________
Correspondence should be sent to Kristiaan D'Août, Laboratory for Functional
Morphology, University of Antwerp (UIA), Universiteitsplein 1, 2610 Wilrijk,
Belgium (e-mail: [email protected])
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measurements on the bipedal and quadrupedal sequence illustrate a clear rolloff pattern starting in most cases from the heel, along the lateral edge of the
foot, to the distalmost toe.
Mots clés : Pan paniscus, locomotion, bipédie, quadrupédie, cinématique,
force de réaction du sol, pédobarographie, zoo.
Key words: Pan paniscus, locomotion, bipedalism, quadrupedalism,
kinematics, ground-reaction force, pedobarography, zoo.
__________
INTRODUCTION
Great apes display a wide variability in locomotor types, e.g., vertical
climbing, brachiation, arboreal scrambling and terrestrial walking, either
quadrupedally or bipedally. Most of these locomotor types have been studied
(to various extents) from a kinesiological point of view. Best studied are
chimpanzees Pan troglodytes (e.g., Elftman & Manter, 1935; Elftman, 1944;
Jenkins, 1972; Kimura, Okada, & Ishida, 1977; Kimura, Okada, Yamazaki, &
Ishida, 1983; Tuttle, Basmajian, & Ishida, 1978; Alexander & Maloiy, 1984;
Ishida, Kumakura, & Kondo, 1985; Okada, 1985; Hunt, 1991; Kimura, 1991,
1992, 1996; Tardieu, Aurengo, & Tardieu, 1993; Shapiro, Anapol, & Jungers,
1997; Doran, 1997; Wunderlich, 1999; Wunderlich & Ford, 2000), but other
species have been studied as well, e.g., bonobos Pan paniscus (Aerts, Van
Damme, Van Elsacker, & Duchène, 2000), gorillas Gorilla gorilla (Tuttle et
al., 1978; Doran, 1997), orangutans Pongo pygmaeus (Tuttle et al., 1978) and
gibbons Hylobates sp. (Kimura et al., 1977, 1983; Ishida et al., 1985; Chang,
Bertram, & Lee, 2000).
The studies mentioned mostly focus on a selected aspect of locomotion,
for instance kinematics (e.g., Okada, 1985), ground-reaction forces (e.g.,
Kimura, 1992), or plantar pressure measurements (e.g., Wunderlich, 1999).
Ideally, the locomotion of apes should be studied using a range of tech-niques
as wide as possible. However, such an integrated approach is not self-evident
since most subjects reside either in situ, or in public zoos.
The purpose of this paper is to present an integrated setup, in a zoo
environment, for combined registration of as much kinesiological information as possible (three-dimensional kinematics, ground-reaction forces,
plantar pressures) with minimal impact on the behavior and daily routine of
the subjects. Preliminary data on bipedal and quadrupedal walking will be
presented, and we will discuss to what extent data from this integrated setup
can be compared to data achieved with the same bonobo population, but
Integrated study of bonobo locomotion
193
under free ranging conditions.
MATERIAL AND METHODS
General description of the setup
An integrated setup, consisting of a horizontal, instrumented walkway
(width, 1 m; length, 8.5 m) and a wall (height, 2 m) was constructed in the
Animal Park of Planckendael in Muizen, Belgium. This setup is further
referred to as the "catwalk" (Figure 1). The bonobo population in
Planckendael (four males, six females) is housed in a purpose-built complex
with two main units (see Van Elsacker, Claes, Melens, Struyf, Vervaecke, &
Walraven, 1993, for details). The first unit is a large indoor playhall that gives
access, through two doors, to the second unit, a 3000-m2 outdoor island
surrounded by a water moat. The catwalk is located at the door closest to the
visitors. When catwalk recordings are being carried out, the other door is
closed and the bonobos have to use the catwalk to go inside or outside.
Kinematics
Kinematic recordings are made by means of two S-VHS cameras (JVC
TK-C1381EG, 50 fields s-1). One camera, perpendicular to the long axis of the
catwalk, is located at a distance of 8.8 m. A second camera, giving frontal or
dorsal views, is aligned with the long axis of the catwalk and located on the
bonobo island, in a purpose-built cage at approximately 6 m from the catwalk
(to the left in Figure 1). Both cameras are positioned fully horizontally with
the optical axis 0.8 m above the catwalk surface.
The luminance (Y) and chrominance (C) signals from both cameras are
split and led separately (using video-grade coaxial cables) to the observatory
on the first floor of the bonobo building (see Figure 1). There the signals are
recorded with a JVC S-VHS recorder (model BR-S800E) or with a DoReMi
V1 digital recorder. All cameras and recorders are gen-locked by means of a
Kramer black-burst generator. The recordings of both cameras are provided
with the same (frame-precise) time code, generated by the JVC recorder.
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Figure 1. Overview of the catwalk setup in Planckendael, seen from the visitor's
point of view.
On the right-hand side of the running track, the door through which the bonobos
leave their indoor playhall can be seen. A second door, closed during recording
sessions, is located behind the catwalk. On the left-hand side of the catwalk, and
behind it, stretches the 3000 m2 bonobo island. The catwalk is constructed on a
rough concrete surface that can be seen in front of it and that was used in a
previous study (Aerts et al., 2000). The middle two meters of the 7 meter-long
catwalk contain the force plates and footscan pressure mats. The window that can
be seen on the left-hand side of the bonobo building is that of the observatory,
where the data from the catwalk are gathered.
Figure 1. Vue d’ensemble de l’installation de la piste de marche à Planckendael,
à partir de l’observatoire des visiteurs.
The registration equipment of the catwalk consists of video equipment (for
kinematic recordings), and built-in equipment (for registration of groundreaction forces and plantar pressures). Poster panels and a video presentation
inform the visitors of the animal park about the setup and its purpose.
Integrated study of bonobo locomotion
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For analysis of selected sequences, the video footage of both cameras is
grabbed, synchronized and digitized using APAS (Ariel Dynamics). For the
present study, we digitized, at 20 ms intervals, the following 20 anatomical
points: crown of the head, chin, and (each time left and right) finger tips,
wrists, elbows, shoulders, hips, knees, ankles, heels, and toe tips. Furthermore, a calibration frame (2 × 1 × 1.5 m), positioned on the catwalk between
recording sessions, was digitized and allowed for scaling and perspective
correction of the digitized images. The APAS system allows the calculation
and presentation of kinesiological variables, such as 3-D dis-placements,
velocities and accelerations of the digitized points, calculation of the center of
mass (if specimen segment data are given), segment and joint angles, etc. It
can reconstruct views that are not available in the original recordings (see
Figure 3).
In this study, we present stick diagrams of one quadrupedal walking
sequence and one bipedal walking sequence of an adult bonobo, and data on
the relationship between speed, stride length, and stride frequency for six
bipedal sequences and six quadrupedal sequences. In order to account for
size differences between individuals, all these factors are made dimension-less
using the principle of dynamic similarity. Dimensionless speed is calculated
as (v2/gl)1/2 with v = absolute speed, g = gravity, and l =, the length from
knee to heel. Stride frequency is dimensionless as such. Stride length was
made dimensionless by dividing by l (see Aerts et al., 2000, for details). These
data are compared with a previous study (Aerts et al., 2000) on the same
bonobo population but under different circumstances, i.e., without the
catwalk setup and on a rough, concrete ground surface. ANCOVA analyses,
with dimensionless speed as a covariate, were carried out to test for statistical
differences between the data from this study and from Aerts et al. (2000)
(Statistica for Windows 5.0).
Ground-reaction forces and plantar pressures
The middle section of the catwalk is equipped with three strain gauge
based force plates (AMTI). Plate "A", which is closest to the bonobo building,
is 1 m long and 0.4 m wide. Plates "B" and "C" (the latter being furthest from
the bonobo building) are 0.5 m long and 0.4 m wide. These plates are bolted
onto heavy steel support bases that are embedded in light concrete. Threedimensional force signals (Fx, Fy, and Fz) and moments signals (Mx, My, and
Mz)
from
these
plates
are
led
to
AMTI
bridge
amplifiers in the observatory (in our setup we used a nominal gain of 4000
and a 1050 Hz low-pass filter).
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On top of each of the force plates, footscan plates (RSScan International,
Belgium) of the same width and length (footscans "A", "B", and "C") are
safely glued, level with the catwalk surface, and the whole walkway surface is
covered with one piece of thin (2 mm) but strong rubber sheet. Each footscan
plate consisted of an array of pressure-sensitive sensors (5 × 7.6 mm). The 1
m plate had 8192 sensors and the 0.5 m plates each had 4096 sensors. The
signals from the footscan plates are led to the observatory. Each footscan
signal, along with the Fx, Fy, and Fz signals of the corresponding AMTI
amplifier, is fed into one of three 3-D boxes (boxes "A", "B", and "C",
RSScan International, Belgium). The rationale for using a combination of one
1 m unit and two 2 m units is the following. On the one hand, the long (1 m)
unit would increase the chance of recording complete footprints (with the
drawback of multiple plate contacts which hamper analysis of groundreaction forces). On the other hand, the two short (0.5 m) units would
increase the chance of recording two subsequent single-foot ground-reaction
forces (easier to analyse, but with the drawback of an increased chance of
incomplete footprints).
In the 3-D boxes, 1000 (for 0.5 m systems) or 500 (for 1 m systems) data
sample sets can be stored. Each data sample set consists of the digi-tized
values (8 bit resolution) of the pressure of each footscan sensor and the Fx,
Fy, and Fz ground-reaction forces. In our setup, we measured at 250 Hz,
which allowed a total recording time of 2 s (unit "A") or 4 s (units "B" and
"C"). The 3-D boxes perform an on-line calibration in which, at each moment
in time, the integrated pressure of all sensors is set equal to the vertical
ground-reaction force (Fz) from the force plate, thus eliminating to a great
extent the error inherent in the plantar pressure measurements. The three 3-D
boxes are equipped with sync-in and sync-out connectors that al-low an
automatic and synchronous start of measures (forces and pressures) in
systems A, B, and C.
After data collection, the data of the 3-D boxes are transferred to
computers "A", "B", and "C" (Apple Macintosh G3) running Footscan
software (version 6.3.1 Multistep). The measurements are visualized and
stored in these computers, and available for later analysis. Analysis may
include playback of pressure patterns, tracking of the displacement of the
center of pressure, time-pressure analysis of selected landmarks or zones
under the foot, etc. In this study, we present preliminary results on the
ground-reaction forces and plantar pressures of one bipedal and one quadrupedal walking sequence. These results should not be considered as characteristic of all bipedal or all quadrupedal sequences.
Integrated study of bonobo locomotion
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RESULTS
Relevant descriptive kinematic variables (dimensionless speed, stride
length and stride frequency; see Alexander & Maloiy, 1984) are calculated for
six bipedal and six quadrupedal sequences from the catwalk setup. They are
compared graphically (Figure 2 A, B) and statistically with previous results on
bonobo walking (Aerts et al., 2000). The average dimensionless speed of the
twelve catwalk sequences (this study) was approximately 30% slower than in
Aerts et al. (2000). The ANCOVA shows that, when ac-counting for speed
differences, curves do not differ significantly (0.18 < p < 0.63). When
bonobos increase walking speed, they increase both stride length and stride
frequency, but for a given speed, bipedal walking uses shorter strides at a
higher frequency.
Figure 3 shows stick-diagrams of bonobos walking bipedally and quadrupedally. The vertical displacement of the center of mass seems limited (Figure
3 A, B), but dorsal-view images (Figure 3 C, D) show considerable lateral
movements of the center of mass. During both gait types, the hip and knee
show considerable angles (Figure 3 E, F), characteristic of the "bent-hip, bentknee" type of locomotion observed in apes.
Ground-reaction force (Figure 4) has limited lateral and fore-aft components. The vertical component (Fz) may show an impact peak (as in Figure
4 B). In the quadrupedal example sequence, there was a clear single peak in
Fz. In the bipedal example sequence, the profile was unclear and three peaks
can be distinguished. Both profiles are unlike the clear double-humped Fz
profile observed in human walking (e.g., Winter, 1990).
The footscan plots in Figure 5 show that the hallux is abducted in the two
gait types, bipedal or quadrupedal. In both cases, the center of pressure
travels along the lateral edge (5th ray) of the foot and may shift towards the
hallux (as in the bipedal sequence) at the end of the stance phase. In general,
the center of pressure travels from the heel to the distalmost toe (in the
direction of movement), although, in the bipedal sequence presented here
(Figure 5 A), initial ground contact is made in the midfoot. Figure 6 shows a
dynamic view of foot roll-off.
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Figure 2. Comparison of dimensionless stride length (panel A) and dimensionless
stride frequency (panel B) between data in Aerts et al. (2000), on a semi-natural
ground surface, and this study (on the catwalk).
Filled symbols, data from Aerts et al. (2000); open symbols, data from this study.
Squares, bipedal walking; diamonds, quadrupedal walking. For both bipedal and
quadrupedal walking, results between Aerts et al. (2000) and this study were not
significantly different (see text).
Figure 2. Comparaison des enjambées (graphe A) et de la fréquence (graphe B)
entre les données de l’étude (sur la piste) et ceux de Aerts et al. (2000) sur un sol
semi-naturel.
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Figure 3. Kinematic overviews of bonobo walking.
A, C, E, quadrupedal walking; B, D, F, bipedal walking. Panels A and B illus-trate
body posture and the path of the center of mass from a lateral view. Panels C and D
show the same from a dorsal view. Panels E and F are superimposed, lateral-view
stick diagrams of approximately one stride. The markers correspond with the head
and the right-hand side of the animal, and with the center of mass. Note the benthip, bent-knee posture in both bipedal and quadrupedal walking.
Figure 3 : Etude cinématique de la marche des bonobos. (A, C, E, marche quadrupède ; B, D, F, marche bipède. Position corporelle et déplacement du centre de
masse : A et B en vue latérale ; C et D : en vue supérieure. E et F : diagram-mes en
bâtons montrant le déplacement des segments du corps en vue latérale approximativement une enjambée.)
If we focus on selected regions of interest under the foot (here, in Figure 7,
for the quadrupedal sequence), the roll-off pattern is clear as well. Figure 7
shows at which fraction of stance there is peak pressure under the selected
zones, and quantifies the magnitude of pressure. Pressure development under
the foot is first and highest under the heel (zones H1 and H2). Pres-sure under
the midfoot point (M1) is considerable and a clear pressure point can be
observed, presumably corresponding with the location of the proxi-mal head
of the 5th metatarsal bone. Pressure under the toes is high; under the 5th toe
(T5) it is nearly as high as peak pressure under the heel.
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Figure 4. Example plots of ground-reaction forces of a single foot for bipedal
walking (panel A) and quadrupedal walking (panel B).
Fx, fore-aft component; Fy, lateral component; Fz, vertical component. Doublestance is approximately the first and the last 15% of contact time, assuming a typical
duty factor of 0.65 (the average found in Aerts et al., 2000).
Figure 4. Graphes des forces de réaction du sol sur le pied durant la marche
bipède (graphe A) et quadrupède (graphe B).
Integrated study of bonobo locomotion
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Figure 5. Example plots of the footscan pressure mats. All plots are maximal
pressures during the ground contact concerned and correspond with the ground
reaction forces in Figure 4.
The dotted lines in the foot plots illustrate the displacement of the center of pressure
(dot interspacing, 4 ms). Note the abducted position of the hallux.
In this particular bipedal footprint (panel A), initial contact is made with the
midfoot, which occurs in some cases. Then the center of pressure quickly moves
towards the heel. Roll-off involves displacement of the center of pressure along the
lateral edge of the foot, down to the 5th metatarsal head. Then, the center of
pressure shifts towards the hallux.
In this particular quadrupedal footprint (panel B), initial contact is made with the
heel (which is also found most often in bipedal walking). Roll-off is lateral as well,
but the hallux receives little pressure.
The handprint (panel C) illustrates pressure distribution under the 2nd phalanges of
fingers II-V during "knuckle walking". In some cases, only two or three fingers are
involved.
It should be stressed that plantar pressure patterns in walking bonobos are very
variable and the footscans shown here are preliminary examples.
Figure 5. Exemples d’enregistrements de la pression des pieds.
Tous les enregistrements correspondent à des pressions maximales enregistrées lors
du contact avec le sol, et expriment les forces de réaction du sol (voir Figure 4).
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Figure 6. Footscan sequences illustrating foot roll-off during bipedal walking
(upper panel) and quadrupedal walking (lower panel).
Time interval between the consecutive plots is 100 ms (i.e., 25 frames) for the
bipedal sequence and 40 ms (i.e., 10 frames) for the quadrupedal sequence. The
homogeneous gray area marks the total footprint observed during complete stance
phase. The gray-scale areas mark the pressure distribution at the very instant in time
(indicated, in ms, in the bottom right corner of each print).
Figure 6. Séquences d’enregistrement de pression plantaires montrant le déroulement du pied durant la marche bipède (en haut) et la marche quadrupède (en
bas).
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Figure 7. Example plots of average pressure under specific zones of the foot as a
function of time.
The footscan used is the same as the one in Figures 4, 5 and 6. The selected zones
of interest are H1, medial side of the heel; H2, lateral side of the heel; M1, midfoot
(proximal head of metatarsal V); T1, hallux; T3-5, toes 3-5. More zones can be
analysed if desired. If the zones are well chosen, their summed plots should closely
resemble the Fz component of the ground-reaction force.
The graphic shows that initial contact is with the lateral heel (peak approx. 150 ms
after initial contact), then the medial heel reaches peak pressure. Next, the midfoot
reaches peak pressure, at midstance. The toes receive pressure last; the last to leave
the ground is the one located the furthest forwards in the direction of movement
(toe III in this case).
Figure 7. Exemples de graphique d’enregistrement de pression dans des zones
spécifiques du pied en fonction du temps. Les données sont les mêmes que celle
des empreintes des Figures 4, 5 et 6.
DISCUSSION
The preliminary results, presented above, show that the integrated
"catwalk" setup allows a simultaneous collection of data (kinematics, groundreaction force and plantar pressure) in a zoo environment. The subjects of our
study appear to show normal locomotor behavior, as is suggested by the fact
that descriptive kinematic data (dimensionless stride length and stride
frequency) from this setup have the same relationship with dimensionless
velocity as previously published relationships, on the same bonobo
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population, under semi-natural conditions.
The data presented in this study are preliminary, and our observations
clearly show that variability in most gait variables is considerable (unpublished data). Therefore, we do not attempt to describe general patterns for
the bonobo in this paper. Nevertheless, it is clear that bonobos walk with a
bent-hip, bent-knee mechanism and with a foot roll-off pattern that travels
from the heel to the toes, where in most cases, the center of pressure runs
along the lateral edge (5th ray) of the foot. During bipedal walking, a double
humped vertical ground-reaction profile (indicating an efficient "inverted
pendulum" gait) is not typical but may occasionally occur.
Since the catwalk setup is highly visible to the visitors of the animal park,
ample information on its purpose and on the ongoing research project is
provided in the neighborhood of the catwalk, by means of a video production
and poster panels. On a regular basis, visitors can attend guided visits to the
observatory while recordings are being made. In this way, the catwalk setup
serves both scientific and educational purposes.
We conclude that data on apes, yielded by means of an integrated zoo
setup, can provide information on many aspects of locomotion that are
otherwise difficult to obtain. If these kinesiological data are supplemented by
morphometrical data and by segment inertial data (see Crompton, Li,
Alexander, Wang, & Günther, 1996, for a technique useable in a zoo), a
profound understanding of the mechanics of locomotion can be achieved.
ACKNOWLEDGEMENTS
We thank Guy Claes and the Planckendael staff for the opportunity to construct
the catwalk, Ludo Wouters and Rudy van der Auwera for help with the technical
realisation, Herman Costima for the educational DVD production, and bonobo
keepers Stéphane Dawance, Harry De Gruyter, Joris Jacobs, and Ludo Van Mirlo
for practical help during recording sessions. Dr. Christine Berge and an anonymous reviewer provided invaluable comments on an earlier version of the
manuscript. This study was funded by project G.0209.99 of the FWO-Vlaanderen.
RÉSUMÉ
Nous décrivons l’installation mise en place dans le parc animalier de
Planckendael (Belgique) pour une étude intégrée de la locomotion terrestre
chez les bonobos (Pan paniscus). L’installation consiste en deux caméras
vidéo orthogonales (50 Hz) et en trois appareillages de mesures synchronisées (250 Hz) incorporés dans le plancher d’une piste de marche. Chaque
Integrated study of bonobo locomotion
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appareillage consiste en une plate-forme de force fonctionnellement associée
à de la pédobarographie à haute résolution spatiale et temporelle.
Les résultats préliminaires montrent que la locomotion terrestre des
bonobos est hautement variable. L’enjambée et la fréquence adoptées en
marches bipède et quadrupède ne diffèrent pas significativement des données récoltées précédemment dans des conditions semi-naturelles. Nous présentons comme exemples les données cinématiques de forces et de pressions
plantaires enregistrées lors d’une séquence bipède et d’une séquence quadrupède. Dans ces analyses préliminaires, les déplacements verticaux du
centre de masse sont limités. Dans les deux cas, les animaux ont adopté une
position "hanche fléchie, genoux fléchis" au cours du cycle qui définit l’allure.
Comme pour les mesures cinématiques, les forces de réaction du sol sont
variables. La courbe "en chapeau" (deux pics de pression) décrite dans la
marche "en pendule inversée" de l’espèce humaine, n’a pas été clairement
observée.
Les mesures de pression plantaire dans la séquence bipède et quadrupède
illustrent clairement le patron de déroulement du pied dont l’appui commence
dans la plupart des cas par le talon, pour se poursuivre ensuite par le bord
latéral du pied, pour finir enfin par l’orteil le plus distal.
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