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Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus).

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 120:373–383 (2003)
Dynamic Plantar Pressure Distribution During Terrestrial
Locomotion of Bonobos (Pan paniscus)
Evie Vereecke,1* Kristiaan D’Août,1 Dirk De Clercq,2 Linda Van Elsacker,1,3 and Peter Aerts1
1
Department of Biology, University of Antwerp, B-2610 Wilrijk, Antwerp, Belgium
Laboratory for Movement and Sport Sciences, Ghent University, B-9000 Ghent, Belgium
3
Royal Zoological Society of Antwerp, B-2018 Antwerp, Belgium
2
KEY WORDS
foot function; bipedal/quadrupedal walking; primate locomotion;
pedobarography
ABSTRACT
We collected high-resolution plantar pressure distributions of seven bonobos during terrestrial bipedal and quadrupedal locomotion (N ⫽ 146). Functional
foot length, degree of hallux abduction, and total contact
time were determined, and plots, showing pressure as a
function of time for six different foot regions, were generated. We also studied five adult humans for comparison
(N ⫽ 13). Both locomotion types of the bonobo show a large
variation in plantar pressure distributions, which could be
due to the interference of instantaneous behavior with
locomotion and differences in walking speed and body
dimensions. The heel and the lateral midfoot typically
touch down simultaneously at initial ground contact in
bipedal and quadrupedal walking of bonobos, in contrast
with the typical heel-strike of human bipedalism. The
center of pressure follows a curved course during quadrupedalism, as a consequence of the medial weight transfer
during mid-stance. Bipedal locomotion of bonobos is characterized by a more plantar positioning of the feet and by
a shorter contact time than during quadrupedal walking,
according to a smaller stride and step length at a higher
frequency. We observed a varus position of the foot with
an abducted hallux, which likely possesses an important
sustaining and stabilizing function during terrestrial locomotion. Am J Phys Anthropol 120:373–383, 2003.
The acquisition of habitual bipedalism is a puzzling aspect of human evolution and, unsuprisingly,
research concerning this topic is quite extensive
(e.g., Susman, 1984; Rose, 1991; Susman and Stern,
1991; Senut, 1992; Wood, 1992; Zihlman, 1992; Jablonski and Chaplin, 1993; Benton, 1997). However,
these investigations are mainly limited to hominid
fossils. We think that a comparative analysis of the
locomotion of extant nonhuman primates can give
valuable information on the mechanics of bipedalism and add to the interpretation of fossil findings.
Since none of the extant apes can be considered as a
perfect model for the hominid ancestor, this research requires data from as many relevant ape
species as possible (Fleagle, 1979, 1999; Fleagle et
al., 1981; Aerts et al., 2000). For several reasons, we
chose to focus on the bonobo (Pan paniscus). First of
all, bonobos are, together with chimpanzees, our
closest living relatives, showing only 1.2% difference
in genetic material with Homo sapiens (Chen and Li,
2001). Secondly, bonobos live in the tropical rainforest, a habitat similar to that of the common ancestor
(Kano, 1992). It seems reasonable to assume that
the bonobo should therefore have a similar morphology as our common ancestor. Analyses of the functional morphology of (pre)hominid fossils and bonobos show that the bonobo likely resembles the
common hominoid ancestor and the early hominids
more than any other African ape species (Zihlman
and Cramer, 1978; Zihlman et al., 1978; McHenry
and Corruccini, 1981; Zihlman, 1984; McHenry,
1984; Kano, 1992). Since we study locomotion and
functional morphology, it is thus meaningful to use
bonobos as a model for the prehominid condition.
Thirdly, bonobos quite often engage in bipedal walking, compared to other great apes (up to 8%; Doran,
1989; Susman et al., 1980; Susman, 1984). And
lastly, most of the current studies apply to common
chimpanzees (e.g., Jenkins, 1972; Bauer, 1977;
Kimura et al., 1977, 1983; Kimura, 1985, 1990,
1996; Ishida et al., 1985; Okada, 1985; Li et al.,
1996), but data on bonobo locomotion and functional
morphology are scarce. With this paper, we hope to
add relevant data to our current knowledge of ape
locomotion.
©
2003 WILEY-LISS, INC.
©
2003 Wiley-Liss, Inc.
Grant Sponsor: FWO-Flanders; Grant number: G.0209.99; Grant
Sponsor: University of Antwerp.
*Correspondence to: Evie Vereecke, Laboratory of Functional Morphology, Department of Biology, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium. E-mail: Evie.Vereecke@ua.ac.be
Received 24 January 2002; accepted 27 June 2002.
DOI 10.1002/ajpa.10163
Published online in Wiley InterScience (www.interscience.wiley.
com).
374
E. VEREECKE ET AL.
TABLE 1. Origin, sex, year of birth, weight, and number of analyzed sequences of different individuals
Number of sequences
Qped
1
Individual (origin)
Dz (wild)
Ki (zoo)
He (wild)
Ho (wild)
Ko (wild)
Re (zoo)
Un (zoo)
Vi (zoo)
Zo (zoo)
Za (zoo)
Total
1
Sex
Year of birth
F
M
F
F
F
M
F
M
F
M
1971
1983
1978
1978
1982
1990
1993
1994
1999
1999
Bped
Weight (kg)
2000
2001
2000
2001
36.3
46.1
37.0
36.7
47.3
34.0
18.5
5.1
5.8
0
14
5
5
7
21
15
8
0
0
75
0
3
2
6
4
11
7
4
0
0
37
0
0
1
12
0
2
0
0
0
0
15
0
2
5
12
0
0
0
0
0
0
19
Wild, born in Democratic Republic of Congo; zoo, born in captivity; Bped, bipedal; Qped, quadrupedal.
This paper fits in current research on terrestrial
walking of bonobos, with the aim of getting a full
insight into their locomotory pattern, with special
emphasis on the differences between bipedalism and
quadrupedalism. Aerts et al. (2000) dealt with the
relations of spatio-temporal gait characteristics and
walking speed. It was demonstrated that smaller
steps at a higher frequency were used during bipedal walking. Furthermore, the spatio-temporal gait
characteristics of bonobos appeared to be highly
comparable with those of other extant homininae. In
order to get a full understanding of bonobo locomotion, an integrated setup in a zoo environment was
constructed to get additional information on groundreaction forces and plantar pressure distributions,
together with three-dimensional (3D) video images
(D’Août et al., 2001). The segment and joint angles of
the hindlimb during terrestrial locomotion of bonobos are described by D’Août et al. (2002). It was
found that the major differences between quadrupedalism and bipedalism are situated proximally
(trunk, thigh, and hip angles), and that the bipedal
walking of bonobos is clearly “bent-hip, bent-knee.”
In continuation of those studies, we wanted to focus
on dynamic plantar pressure distributions during
terrestrial walking of bonobos.
So far, only a few studies have collected plantar
pressure data of primates. Since the late nineteenth
century, when Carlet (1872) and Marey (1873) developed the first method to examine plantar pressures, the techniques for the sampling of plantar
pressure profiles have been ameliorated continuously, with the eventual development of pressure
mats and pressure sensors in the last few decades.
The field of application was mainly restricted to the
medical world and to sport sciences. However, the
setup used in this study was developed not only for
medical goals, but also for acquiring quantitative
measurements. Elftman and Manter (1935; see also
Elftman, 1944) were the first researchers who made
a comparison between human and chimpanzee (Pan
troglodytes) bipedalism on the basis of plantar pressure distributions. Recently, Wunderlich (1999, using 16 ⫻ 16 cm pressure mats and sampling at 11
Hz; see also Wunderlich and Ford, 2000) made an
extensive comparison between plantar pressure distributions of different primate species, including
common chimpanzees. To date no study has focused
on the bonobo, despite the notion that this may be an
especially interesting model for our common ancestor among the living apes (Coolidge, 1933; Zihlman
and Cramer, 1978). In the current study, we focus on
the plantar pressure distributions, hallux function,
and other pedal characteristics during terrestrial
walking of the bonobo. We examine if general roll-off
patterns exist for bonobos; what the differences are
between bipedal and quadrupedal walking; and how
they compare to the human pattern.
MATERIALS AND METHODS
Ten bonobos are held in seminatural circumstances on the bonobo island of the animal park
Planckendael in Muizen, Belgium (Van Elsacker et
al., 1993). The data used in this study are taken
from seven bonobos of this group (Table 1). No samples were taken from the oldest and the two youngest bonobos. The data were collected during July,
August, and September 2000 (47 recording days),
and during July, August, September, and October
2001 (36 recording days).
A 7-m-long ⫻ 1-m-wide horizontal catwalk was
built on the bonobo island, equipped with three force
plates and three pressure distribution platforms,
two of 0.5 ⫻ 0.4 m (units B and C: 64 ⫻ 64 pressure
sensors) and one of 1.0 ⫻ 0.4 m (unit A: 128 ⫻ 64
pressure sensors) in each case. These were built in a
concrete construction and covered with a rubber
sheet. A reference wall 7-m-long ⫻ 2-m-high was set
behind the catwalk, provided with a reference grid.
The wall is set vertically along the catwalk, but the
lowest 0.4 m is set at an angle of 45° with the
catwalk, to offer enough space for the bonobos to
move. The three force plates (AMTI, Advanced Mechanical Technology, Inc., excitation voltage 10 V
nominal) give us the 3D ground reaction forces Fx,
lateral force (towards the waterside); Fy, longitudinal force (towards the island); and Fz, vertical force
(downwards). Dynamic plantar pressure measure-
PLANTAR PRESSURE OF BONOBOS
ment is performed at high temporal and spatial resolution (250-Hz sampling and 16,384 pressure sensors of 0.375 cm2), using three pressure mats
(RSscan International) which are secured onto the
force plates. The pressures are calibrated online
with the ground reaction forces, allowing an accurate pressure sampling, and the three measuring
systems are synchronized. Recordings as well as
further data processing are carried out by means of
Footscan mst software 6.2 and 6.3 (RSscan International). Two S-VHS cameras (50 Hz) were set perpendicular to each other, to record the lateral and
frontal view of the catwalk (for more details, see D’
Août et al., 2001).
On each recording day, the amplifiers were balanced, the force plates and the pressure mats were
calibrated, and the catwalk was checked. Subsequently, the bonobos were released on the island,
and they could choose freely how and when to walk
over the catwalk. Because they seldom walked bipedally over the catwalk, they were encouraged to do
so by throwing them food and giving them plastic
casks. This is comparable with the locomotory behavior of wild bonobos, which use bipedalism when
carrying food and other objects (Kano, 1992). Since
we worked in zoo circumstances, direct contact with
the animals was prohibited, which resulted in a
relatively small number of bipedal footprints sampled. Each time a bonobo walked (bipedally or quadrupedally) over the catwalk, the force plates and
the pressure mats were activated. The lateral and
frontal views of the catwalk were simultaneously
videotaped. Specific weather conditions that could
influence measurements were noted (e.g., rain).
For analysis, we selected sequences (N ⫽ 146)
where the force output was recorded during whole
ground contact and where the pressure profile (or
footscan image) showed at least a complete foot. The
center of pressure (COP) during contact time was
calculated as a function of time for every footscan
image. Several measurements were taken on the
pressure profiles (Fig. 1a; only for the data collected
in 2000, N ⫽ 90): 1) the functional foot length, L, i.e.,
the distance between the most proximal point of the
heel to the most distal point of digit II; 2) the degree
of abduction, B, i.e., the angle between the length
axis of digit I and digit II; 3) the contact time, t, i.e.,
the time between initial foot contact and toe-off; and
4) the velocity, v, estimated on the basis of lateral
video images if these were available (Table 2a,b).
We defined six foot regions on the basis of the
functional morphology of the bonobo foot: 1) the heel
(H1 and H2, 6.750 cm2), 2) the lateral midfoot (V2,
3.375 cm2), 3) the medial midfoot (V1, 3.375 cm2), 4)
the lateral metatarsal heads (M II–V; 13.500 cm2),
5) the lateral toes (T II–V, 13.500 cm2), and 6) the
hallux (M I and T I; 6.750 cm2; see Fig. 1b).
For every foot region, the average pressure was
plotted as a function of time, which was normalized
against the duration of ground contact (total duration of stance phase ⫽ 100%). Impulses were calcu-
375
Fig. 1. a: Example of footscan image, recorded by footscan
pressure mats, showing maximal pressures under a right bonobo
foot during ground contact in a quadrupedal walking sequence.
Dotted line in foot illustrates displacement of center of pressure
(dot interspace, 4 msec). Two measurements are taken on the
profiles, i.e., functional foot length, represented by line L, and
degree of abduction, i.e., angle B between length axis of hallux
and digit II (line L). b: Footscan image, showing assessment of 14
foot regions: H1, medial heel; H2, lateral heel; V1, medial midfoot; V2, lateral midfoot; M1–M5, metatarsal heads I–V; T1–T5,
phalanges I–V. In this example there is no contact of the second
and third metatarsal heads, and of the second toe.
lated as the time integral of the vertical force (i.e.,
pressure (N/cm2)* area (cm2)). Relative impulses are
the impulses divided by the total impulse under the
foot. Relative peak pressures under the metatarsal
heads and toes were calculated as maximal pressures normalized for body weight. We processed 13
pressure profiles of five nonpathological, adult humans following the same procedure, for comparison.
376
E. VEREECKE ET AL.
TABLE 2A. Average (X) and standard deviation (SD) of
functional foot length, degree of abduction, and total contact
time during quadrupedal terrestrial locomotion
Individual
N
Foot length, X ⫾
SD (10⫺2 m)
Abduction,
X ⫾ SD (°)
Contact time,
X ⫾ SD (sec)
He
Ho
Ki
Ko
Re
Un
Vi
Total
5
5
14
7
21
15
8
75
19.7 ⫾ 1.0
17.4 ⫾ 2.3
17.6 ⫾ 1.1
21.1 ⫾ 0.9
20.5 ⫾ 1.3
19.7 ⫾ 1.1
17.2 ⫾ 1.8
19.3 ⫾ 1.9
29.2 ⫾ 9.9
31.7 ⫾ 13.5
33.4 ⫾ 6.2
41.1 ⫾ 3.0
24.3 ⫾ 6.2
13.9 ⫾ 7.5
52.1 ⫾ 18.7
28.9 ⫾ 14.4
0.895 ⫾ 0.139
0.865 ⫾ 0.448
0.669 ⫾ 0.076
0.847 ⫾ 0.298
0.913 ⫾ 0.189
0.667 ⫾ 0.090
0.607 ⫾ 0.089
0.775 ⫾ 0.217
TABLE 2B. Average (X) and standard deviation (SD) of
functional foot length, degree of abduction, and total contact
time during bipedal terrestrial locomotion
Individual
N
Foot length X ⫾
SD (10⫺2 m)
He
Ho
Re
Total
1
12
2
15
18.0
19.3 ⫾ 2.3
22.2
19.4 ⫾ 2.5
Abduction,
X ⫾ SD (°)
28.0 ⫾ 10.8
28.0 ⫾ 10.8
Contact time,
X ⫾ SD (sec)
0.528
0.623 ⫾ 0.318
0.274 ⫾ 0.150
0.570 ⫾ 0.310
These human footscan images were collected at the
Laboratory for Movement and Sport Sciences, University of Ghent (Ghent, Belgium).
Statistical analyses were executed on total contact
time, degree of hallux abduction, and relative impulses. We tested for a difference between humans
and bonobos and between quadrupedalism and bipedalism in bonobos. The data are not paired, and
are normally distributed (Shapiro-Wilks, 0.9 ⬍ W ⬍
0.95), so we could use the parametric Student’s t-test
(Statistica 5.0 for Windows). This t-test was also
used to analyze the relative peak pressures under
the metatarsals and toes. Furthermore, the Pearson
product moment correlation coefficient between degree of hallux abduction and relative peak pressure
under the hallux (i.e., maximal pressure/body
weight) was calculated from the mean values of all
seven animals (Statistica 5.0 for Windows).
RESULTS
Our results consist of a general description of the
plantar pressures of quadrupedal and bipedal walking of bonobos, together with a short description of
human bipedalism. The latter does not contain new
findings, but we will use this description in our
comparison with the collected data of the bonobos.
We found that the center of pressure (COP) follows a typical curved course during quadrupedal
walking of bonobos (Fig. 2a). This is caused by a
footfall pattern in which the heel and lateral midfoot
touch down simultaneously at the beginning of the
stance phase, followed by an anterior progression of
the COP during foot-flat and mid-stance, and by a
medial transfer of pressure across the metatarsal
heads at heel-off. At toe-off, the lateral toes and/or
the hallux leave the substrate last. In almost all
cases (67/75) there is an important pressure region
under the lateral midfoot, near the tuberosity of the
Fig. 2. Examples of footscan images during quadrupedal
(a– c) and bipedal walking (d) of bonobos. Plantar pressure profiles in a and d are from a left bonobo foot, those in b and c from
a right bonobo foot. During quadrupedal locomotion (a– c), initial
contact is made by the heel. Then the center of pressure moves
anteriorly towards the metatarsal heads and lateral toes, and
eventually bends towards the hallux. During bipedalism (d), initial contact is made by the lateral midfoot and the center of
pressure moves eventually towards the hallux. Note the variability in plantar pressure distributions, with a V-curved pattern in
b and an almost straight course of center of pressure (indicated by
dotted line) in c, in contrast with the general pattern with a
curved course of center of pressure, shown in a.
metatarsal V head. This region of pressure was even
present after the heel left the substrate (heel-off).
However, there is high variability of footfall patterns during quadrupedal walking. In some cases
(20/75), an almost straight course of the COP was
observed, starting from the lateral side of the heel
and travelling to metatarsal and digit II (Fig. 2c).
Occasionally (5/75), the hallux hits the ground first
and/or the COP follows a V-curved course (17/75;
Fig. 2b). The order in which the different foot regions, especially the metatarsals and the toes, touch
down is also very variable. As a consequence of the
varus position of the foot, i.e., the inverted position
of the foot with curved toes, there is often no contact
from the metatarsal heads II–III and the medial
midfoot with the ground (Fig. 3a).
The plots of pressure as function of time give
following results for quadrupedalism (Fig. 4a).
There is generally a marked peak pressure under
the heel at initial contact, which is larger than the
PLANTAR PRESSURE OF BONOBOS
377
Fig. 3. Examples of roll-off patterns of left foot during quadrupedal (a) and bipedal (b) walking of a bonobo and during
human bipedalism (c). Progress in time is indicated in milliseconds above every footscan image. In quadrupedal footprint (a),
the heel and lateral midfoot touch down simultaneously, then
medial midfoot and lateral toes touch down, and finally the hallux
hits the substrate. In the bipedal footprint of the bonobo (b), the
heel and hallux hit the ground first, and the foot rolls mediolaterally over the lateral toes. In a typical human footfall (c), initial
contact is made by the heel, then the lateral midfoot makes
contact with the substrate, and finally the metatarsal heads and
toes make touchdown. Toe-off generally occurs through the big
toe.
peak pressure under the lateral toes at toe-off. On
average, the pressure under the hallux is larger
than that under the lateral toes during toe-off, although 4 of the 7 individuals are characterized by a
pressure under the hallux, which is smaller or equal
to the pressure under the lateral toes. The other 3
individuals (Ho, Ko, and Vi) have markedly larger
pressure under the hallux than under the lateral
toes. Two of those individuals (Ko and Ho) are also
characterized by a high degree of abduction of the
hallux (Table 4), and therefore we examined
whether a high degree of abduction correlates with a
higher maximum peak pressure under the hallux. A
correlation coefficient between the degree of hallux
abduction and the relative peak pressure under the
hallux (maximum pressure divided by body weight)
was defined, but this was not found to be statistically significant (Pearson product moment correlation coefficient, r ⫽ 0.72, N ⫽ 7, P ⫽ 0.067).
The course of the COP seems even more variable
during bipedal locomotion. In most cases (10/15), the
COP starts at the lateral side, somewhat before the
calcaneus, and travels further anteriorly, under the
lateral or central part of the foot. Near the metatarsal heads, the COP stagnates and eventually bends
off towards the hallux, but we also observed (4/15) a
V-curved course of the COP (Fig. 2d). During bipedalism, the hallux usually hits the ground earlier
than the lateral toes (Fig. 3b).
Fig. 4. Average pressure (N/cm2) for six different foot regions
as a function of time (%) during quadrupedal (a) and bipedal (b)
walking of bonobos, and during human bipedalism (c). Different
foot regions are: H, heel; V1, medial midfoot; V2, lateral midfoot;
M, metatarsal heads II–V; T, lateral toes II–V; Hallux, metatarsal I head and digit I. Note apparent peak pressure under the heel
in a and c, and absence of such a peak pressure in b. Compare also
the relative high pressure under the lateral midfoot, which remains after heel-off (pressure under heel ⬎ 0 N/cm2) in a and b,
with the relatively low pressure seen in c, which disappears at
heel-off.
Graphs of bipedal walking sequences, in which
pressure is plotted against time, show a very irregular pattern where every foot region touches the
ground during 90 –100% of the total contact time
(Fig. 4b). A clear peak pressure under the heel is
absent, and the heel occasionally touches down in
the second half of the stance phase. Pressure distributions under the heel, medial midfoot, metatarsal
heads, and hallux are relatively constant throughout the stance phase. Compared with quadrupedalism, there is a more plantar configuration of the foot
during bipedal locomotion. At toe-off there is a pressure under the lateral toes, but a peak pressure
under the hallux is absent.
The human footfall pattern is rather stereotyped
and is characterized by a slightly curved course of
378
E. VEREECKE ET AL.
where none of the foot regions was significantly different from the other regions. Finally, we investigated the differences in relative peak pressure under the metatarsals, toes, and digits. The pressure
under the fifth metatarsal is significantly higher
than under central metatarsals II and III (P ⬎ 0.001
and P ⬍ 0.01, respectively), but did not differ significantly from the first metatarsal (P ⬎ 0.1). The relative peak pressure under the first toe was, however, significantly higher than under the second and
fifth toes (P ⬍ 0.01 and P ⬍ 0.05). The relative peak
pressure under the second digit is significantly
smaller than under the other digits.
DISCUSSION
Fig. 5. Example of footscan image, showing maximal pressures under a left human foot during ground contact in a bipedal
walking sequence. Dotted line in foot illustrates displacement of
center of pressure (dot interspace, 4 msec).
the COP. This point runs from the heel over the
metatarsal II head and towards the hallucal digit (or
eventually towards digit II) during stance phase
(Fig. 5). At heel-strike only the heel touches down, at
foot-flat the lateral midfoot and metatarsal heads
touch down, and lastly, the lateral toes and hallux
touch down (Fig. 4c). In the second half of the stance
phase, the pressure under the metatarsal heads is
larger than under the hallux, and this in turn is
larger than the pressure under the lateral toes (Fig.
4c). For more detailed descriptions, see Inman et al.
(1981), Perry (1992), Aiello and Dean (1996), and
Whittle (1996).
We executed some statistical analyses (Student’s
t-test) to test the significance of hallucal abduction
and contact time, in order to get a more quantified
image of the different gait types (Table 2a,b). We did
not find a significant difference in degree of abduction of the hallux between bipedal and quadrupedal
locomotion (P ⬎ 0.1; Table 3). The total contact time
of the foot during stance phase, i.e., the time between initial contact and toe-off, is significantly
shorter during bipedalism than during quadrupedalism (t ⫽ ⫺3.09, df ⫽ 88, P ⬍ 0.005; Table 3).
There is no significant difference in contact time
between the bipedalism of bonobos and humans (t ⫽
⫺0.49, df ⫽ 26, P ⬍ 0.1; Table 3). However, the
contact time during quadrupedal locomotion of the
bonobo is significantly larger than during human
bipedalism (t ⫽ 2.67, df ⫽ 86, P ⬍ 0.01; Table 3). The
relative impulses were also statistically tested (Student’s t-test), and there appeared to be no significant
difference between bipedalism and quadrupedalism
of bonobos and human bipedalism. Within a gait
type there were significant differences in regional
relative impulses, except for bonobo bipedalism,
Our results point to some differences between
quadrupedalism and bipedalism of bonobos, and
lead to the formulation of some questions that are
discussed below.
Comparisons between different gait types
Despite the highly variable bipedal pattern of the
bonobo, we were able to detect some differences between the quadrupedal and bipedal locomotion of
bonobos. Moreover, we could make a comparison
with the human pedobarographic pattern.
The total contact time of the bonobo foot during
bipedal walking is significantly smaller than the
contact time during quadrupedal walking. This is in
accordance with the smaller step length and higher
step frequency of bonobo bipedalism, as previously
described by Aerts et al. (2000). The relatively constant pressure under the heel, medial midfoot, metatarsal heads, and hallux through stance phase, together with the comparable relative impulses under
the foot regions and the absence of a peak pressure
under the heel at initial contact, point to a flatter
and more plantar configuration of the feet during
bipedal bouts. This increases the supporting surface
of the foot, and thus likely helps to obtain stability
and maintain balance during bipedal locomotion.
The plantar pressure distribution of human bipedalism is clearly more stereotyped than that of bonobos. In humans, only the heel touches the ground
at heel-strike, followed by the lateral midfoot and
forefoot. This is in contrast with the pattern in bonobo walking, where the heel and lateral midfoot
typically touch down simultaneously, which is reflected in the distribution of fat tissue over the lateral and back part of the foot sole (the heel pad,
personal observations). As a consequence of the
presence of a plantar longitudinal arch in the human foot (Aiello and Dean, 1996; Whittle, 1996),
there is no contact from the medial midfoot with the
substrate (in nonpathological, adult humans). In bonobos, in which a longitudinal arch is absent (personal observations), contact of the medial midfoot is
variable, but we never observed a high loading of the
medial part of the bonobo foot.
379
PLANTAR PRESSURE OF BONOBOS
TABLE 3. Results of Student’s t-test
Abduction Q vs. B
Contact time Q vs. B
Contact time B vs. H
Contact time Q vs. H
1
Q
B
28.9 ⫾ 14.4
0.775 ⫾ 0.217
28.0 ⫾ 10.8
0.570 ⫾ 0.310
0.570 ⫾ 0.310
0.775 ⫾ 0.217
H
T
df
P
0.613 ⫾ 0.059
0.613 ⫾ 0.059
0.21
⫺3.09
⫺0.49
2.67
84
88
26
86
0.83
0.003
0.6
0.009
Q, quadrupedalism, bonobo (N ⫽ 75); B, bipedalism, bonobo (N ⫽ 15); H, human bipedalism (N ⫽ 13).
TABLE 4. Average pressure (X), standard deviation (SD), and maximal pressure/body mass (MAX/MASS) under hallux
for all individuals during quadrupedal locomotion (N ⫽ 75)
Individual
He
Ho
Ki
Ko
Re
Un
Vi
Total
Body mass (kg)
Abduction (°)
X ⫾ SD (N/cm2)
MAX/MASS
46.1
37.0
36.3
36.7
47.3
34.0
18.5
36.6 ⫾ 9.5
29.2 ⫾ 9.9
31.7 ⫾ 13.5
33.4 ⫾ 6.2
41.1 ⫾ 3.0
24.3 ⫾ 6.2
13.9 ⫾ 7.5
52.1 ⫾ 18.7
28.9 ⫾ 14.4
6.02 ⫾ 6.12
23.14 ⫾ 15.15
4.85 ⫾ 5.34
13.10 ⫾ 10.89
5.06 ⫾ 6.23
7.73 ⫾ 5.61
7.35 ⫾ 12.27
9.61 ⫾ 6.59
0.17
0.60
0.32
0.49
0.29
0.22
0.59
0.38 ⫾ 0.18
Variability of plantar pressure distribution
in bonobos
We observed a large interindividual variation in
plantar pressure distributions of terrestrial walking
of bonobos, but within an individual the footfall pattern seems relatively stable, such that it is possible
to recognize the individual on the basis of footscan
images. When variation within an individual is detected, this can often be ascribed to the occurrence of
a different pattern for the left and right foot.
For terrestrial quadrupedalism this variability is
probably a consequence of oblique walking in bonobos (see also D’ Août et al., 2002). In this type of gait,
the trunk is held at an angle to the direction of
travel. In combination with overstriding, this results
in a foot contact pattern where one foot is placed
outside the ispilateral hand, and the other foot is
placed inside the ipsilateral hand (i.e., between the
two hands). The foot that is placed inside the ipsilateral hand is the inside foot and will show a different contact pattern than the outside foot. Moreover, there seems to be an individual preference for
using a particular hindlimb as the inside or outside
hindlimb. This description is in accordance with the
typical walking gait of other great apes (Gorilla
gorilla, Pan troglodytes, and Pongo pygmaeus), as
previously described by Hildebrand (1967) and
Reynolds (1985).
For bonobo bipedalism, the intraindividual variability in pressure patterns may be due to the fact
that bipedalism is used only occasionally. Footfall
patterns observed during the first weeks of bipedal
walking of human toddlers also show high variability (A. Hallemans, personal communication). Besides, the interference of instantaneous behavior
with locomotion, as well as the differences in walking speed and body dimensions, could also explain
part of the observed variability in the terrestrial
walking of bonobos.
It is necessary to investigate if the large interindividual variability is inherent to the bipedalism of
bonobos or if it is only a consequence of the relatively
small sample size. In future research it should be
attempted to collect a large data set of bipedal sequences, although in practice this is not a trivial
undertaking.
We observed an alternative type of foot contact
during the bipedal and quadrupedal locomotion of
several individuals. We call this the toed-in footfall
pattern, because the hallux hits the ground first
(pointed to the inside) and the foot rolls mediolaterally over its lateral toes. This pattern was also described for common chimpanzees, but was considered an individual anomaly, since it was only
observed in 18% of the quadrupedal steps by one
animal and almost exclusively for the outside foot
(Wunderlich, 1999). The fact that this kind of foot
contact was observed by different researchers in bonobos, as well as in chimpanzees, indicates that this
is not an anomaly, but an alternative footfall type,
which is preferred to the standard pattern in certain
situations. Further research could reveal if this pattern is correlated with a particular (inside or outside) hindlimb during oblique walking.
Pressure distribution under the
metatarsal heads
The quadrupedal footfall pattern of bonobos is
generally in accordance with previous descriptions
(Langdon, 1986; Wunderlich, 1999) of quadrupedal
locomotion of the common chimpanzee, and shows
some similarities with the human bipedal pattern.
Wunderlich (1999) quantified the pressure distribution under the metatarsal heads and found that the
pressure under metatarsal head III was significantly higher than under metatarsal heads II and V,
and that the highest pressure always occurs under
380
E. VEREECKE ET AL.
metatarsal I (significantly higher than under M II,
M IV, and M V).
However, if we look at the pressure distribution
under the metatarsal heads in our sequences, we
observe a totally different pattern, in which the
highest pressures are measured under the fifth
metatarsal head and IV, and the lowest pressures
are measured under metatarsals III and II (Fig. 7).
We feel this could be ascribed to the varus position of
the foot with curved lateral toes. In this position, the
lateral border of the foot (M IV and M V) receives
most of the pressure, with a minor loading of the
medial metatarsal heads (M II and M III). If we look
at peak pressures under the digits (metatarsals and
phalanges), the hallux receives the highest pressure
and the second digit the lowest (P ⬍ 0.5) of all digits
(Fig. 7). For the hallux, 74% of the peak pressure is
generated by the phalanges, and only 26% by the
first metatarsal head. The relatively low pressure
that we observed under the head of metatarsal I is
thus combined with a higher loading of the distal
hallucal phalanx.
These findings point to a predominantly lateral
pressure distribution under the foot, with a medial
shift towards the hallucal phalanges at the end of
stance phase. The apparent differences between our
pattern and that described by Wunderlich (1999)
cannot be ascribed to differences in the substrate,
since both studies used a wooden walkway covered
with a rubber sheet. However, because Wunderlich
(1999) used small pressure mats (16 ⫻ 16 cm), she
composed multiple steps to get the pressure distribution under the whole foot. This might have biased
the data, since contact of each foot region is assumed
for every step, which is not representative under
real conditions. This could explain the description of
a more plantar foot posture with high pressures
under the third metatarsal.
General roll-off pattern for bonobos
and humans
Toe-off generally occurs through the longest digit,
i.e., digit II in bonobos and digit I or II in humans,
according to the prediction of the “line of leverage”
theory (Morton, 1924; Wunderlich, 1999). Morton
(1999) defines a humanoid line of leverage for apes
and humans that lies between digit I and II, according to the most distally located metatarsal head.
Metatarsal II is, indeed, longest in humans and
bonobos, but in all hominoids, except humans, the
third proximal phalanx is the longest of all phalanges. This results in a configuration in which the
third toe is more distally extended than the other
toes. However, this is only the case in a position in
which the foot sole is placed flatly on the substrate,
as in humans. Bonobos and chimpanzees often use
an “inverted” foot posture with curved lateral toes
and an abducted hallux, so that the hallux reaches
further distally than the lateral toes. This could
explain why bonobos often roll-off through the hallux and not through the third digit. We can therefore
postulate that both in bonobos and in humans, rolloff occurs through the toe that is most distally located
in the applied foot posture. In bonobos, this is variable, and toe-off occurs with digits I, II, or III. In
humans this variation is smaller, and toe-off occurs
with digits I or II.
The speed effect
Walking speed influences foot-loading patterns,
and it is therefore important to take velocity into
account in gait analyses (Rosenbaum et al., 1994).
However, considering the limitations of working in a
zoo environment, it was not possible to make an
extensive study of the effect of speed on plantar
pressure distributions. To get an impression of the
influence of speed, we analyzed the relationship between contact time and peak pressure for each foot
region for two individuals. We used contact time as
a measure of speed, since we did not dispose of
walking speed data for all sequences. The graphs did
not show a consistent pattern in which peak pressures increased with decreasing contact time. We
think that it is beneficial to look at the speed effect
in more depth, and we plan to do so in future research with more suitable data.
Are bonobos plantigrade?
There have been numerous discussions about
whether or not the terrestrial locomotion of the African great apes is plantigrade. According to Morton
(1922, 1924), only humans are truly plantigrade,
while Keith (1929) believed that all apes are plantigrade. Tuttle (1970) described chimpanzees and gorillas as basically plantigrade. Gebo (1992, 1993)
saw plantigradism as a synapomorphy of the African
great apes and humans, associated with a terrestrial
way of life. Gebo (1997, 1993) assumed that this
points to a stage of terrestrial quadrupedalism in
the evolution of human bipedalism (contra Prost,
1980). However, Meldrum (1993) claimed that heel
contact is common in many primates, and that plantigrady is a primitive condition. It is obvious that we
need some clarity on this subject.
The main problem is the lack of a clear-cut definition of the term “plantigrady.” Schmitt and Larson
(1995) offered a valuable contribution to this topic.
Schmitt and Larson (1995) gave a comprehensive
overview of the recent debates on heel contact and
plantigrady. The patterns of heel contact of 30 primate species were analyzed and classified in three
distinct categories, namely: 1) digitigrade; 2) semiplantigrade; and 3) plantigrade. They defined plantigrade, as “a foot position in which there is a complete heel contact with the substrate at some point
during support phase of locomotion,” and make a
division into “heel-strike” and “mid-foot/heel” plantigrady. If we follow this definition, we should classify the bonobo as “heel-strike plantigrade,” since P.
paniscus shows a clear heel-strike at initial ground
contact. However, the bonobo foot is placed on the
PLANTAR PRESSURE OF BONOBOS
substrate in a somewhat different configuration
than in humans.
Elftman and Manter (1935) demonstrated that
the initial foot contact of common chimpanzees (Pan
troglodytes), where heel and lateral midfoot touch
down simultaneously, is different from the typical
human heel-strike, where only the heel touches
down (at least in 75% of cases; Kerr et al., 1983;
Aerts and De Clercq, 1993; De Clercq et al., 1994).
This is also the most striking difference that we
observed in this study between the footfall patterns
of humans and bonobos.
In the beginning of the twentieth century it was
observed that apes possess an inverted position of
the foot during climbing, whereas humans show an
eversion of the foot during bipedalism (Wood-Jones,
1916, in Wunderlich, 1999; p. 10). The inversion that
is found in primates during climbing is retained
during terrestrial locomotion, and has been called
the varus position of the foot. We observed, indeed,
that bonobos walk with “inverted” feet. In this position, the lateral toes are curved, letting the weight
rest on the dorsal surface of the middle and distal
phalanges (instead of on the plantar side of the
distal phalanges). Some individuals (Ko and Vi)
have also been noticed to place the feet completely
flat on the ground with extended toes, in which the
distal phalanges touch the ground with their plantar
surfaces, similar to the human condition.
Within the clear definition of plantigrady given by
Schmitt and Larson (1995), we feel that it is confusing
to classify the great apes, and thus bonobos, in the
same group as humans as being “heel-strike plantigrade,” since there is a clear difference between their
foot positions. Plantigrady is a foot position in which
the plantar surface of the foot is in contact with the
substrate; hence the term, which is not typically the
case in the great apes. Due to the inversion of the foot
of bonobos, and other great apes, it is mainly the lateral side of the foot which is frequently in contact with
the substrate. We should be able to make a distinction
between those different foot positions, which is not
possible with the current definitions. In fact, the term
“plantigrady” only fully describes the human foot position, but regarding the prevailing definitions, it
would certainly be confusing to restrict the term “plantigrade” to the human condition. Instead, we suggest
dividing the existing term “heel-strike plantigrady”
into an inverted type for the foot position of the great
apes, and a full-contact type for humans. The “fullcontact” heel-strike plantigrady of the human foot is
an apparent specialization to habitual bipedalism, and
therefore an apomorphy of the homininae. Heel strike,
and not “plantigrady” per se, may be a synapomorphy
for the great apes, and is probably related to increased
terrestrial habitat use.
What is the function of the hallux in terrestrial
locomotion of the bonobo?
In our study, we did not find significantly greater
abduction of the hallux during bipedalism. However,
381
Fig. 6. Hatched, shaded, and dotted bars show mean relative
impulses under six foot regions for, respectively, quadrupedal
walking of bonobos, bipedal walking of bonobos, and human bipedalism. Vertical lines indicate standard deviations. H heel; V1,
medial midfoot; V2, lateral midfoot; M, metatarsal heads (II–V);
T, lateral toes (II–V); Hallux, M1 ⫹ T1; Qped, bonobo quadrupedalism; Bped, bonobo bipedalism; Human human bipedalism.
this was observed in the field during arboreal bipedal locomotion of bonobos (Susman et al., 1980), and
concerned walking over a large branch (⬎20 cm). We
used a flat substrate in our setup, which may offer
greater stability than a round branch. So it seems
that abduction of the hallux is less necessary during
terrestrial bipedalism, because other mechanisms,
e.g., a more plantar position of the foot, are likely
sufficient to keep balance.
Nevertheless, some researchers (e.g., Meldrum,
1991; Wunderlich, 1999) have postulated that the
hallux has a negligible function in the terrestrial
locomotion of primates, because they observed a
large variation in degree of abduction of the hallux.
We found, indeed, high variation in degree of abduction (Table 4), especially between individuals, but
also between the left and the right foot of the same
individual (“inner” and “outer” foot). There does not
seem to be a correlation between degree of abduction
and age or body mass, because a high degree of
abduction of the hallux has been observed both in
juveniles and in adults. Despite this high variation,
the hallux might possess an important sustaining
and stabilizing function, since there is an important
pressure region under the hallux during stance
phase. To get an idea of the propulsive function of
the hallux of bonobos compared to humans, we calculated relative impulses from the regional pressure
data and, as expected, the relative impulse under
the bonobo hallux is smaller than under the human
hallux, and is also smaller than under the lateral
toes of the bonobo, although none of these differences are statistically significant (Fig. 6). In humans, propulsion at toe-off is thus mainly generated
by the hallux, whereas in bonobos, propulsion is
primarly generated by the lateral toes. It seems
likely that the propulsive function of the hallux is
less crucial during bonobo walking than during human (habitual) bipedalism, where the hallux generates high forces at toe-off.
382
E. VEREECKE ET AL.
balance during bipedalism. In both gait types, the heel
and lateral midfoot typically touch down simultaneously at initial contact, and a midtarsal break is
present. The foot position can be categorized as inverted heel-strike plantigrady, and the hallux has an
important stabilizing and sustaining function. The observed variability of the collected plantar pressure profiles may be due to the interference of instantaneous
behavior with locomotion, and differences in walking
speed and body mass.
ACKNOWLEDGMENTS
Fig. 7. Bar-chart shows relative peak pressure (peak pressure/body weight, N/cm2kg) under digits during quadrupedal
walking of bonobos (N ⫽ 61). Shaded bars represent relative peak
pressures measured under toes (T). Hatched bars represent relative peak pressures measured under metatarsal heads (M). D1–
D5, digits I–V (and D ⫽ M ⫹ T).
Which joint causes the midtarsal break during
terrestrial locomotion?
A midtarsal break occurs as a consequence of a
flexible midfoot. Due to this considerable flexibility,
the heel can be lifted before the midfoot leaves the
ground. This is only occasionally seen in humans (e.g.,
in basketball players; M. Lafortune, Nike Inc., personal communication), but has repeatedly been described for primates (Elftman and Manter, 1935; Aiello and Dean, 1996; Wunderlich, 1999, D’ Août el al.,
2002). In our study, we observed a distinct pressure
region under the lateral midfoot on the plantar pressure profiles of bonobo feet, which remains present
after heel-off. The bonobo foot thus clearly possesses a
midtarsal break. Nevertheless, it is still unclear which
tarsal joint causes this midtarsal break. Classically,
the calcaneo-cuboid joint is assumed to be responsible
for this apparent flexibility of the midfoot (Elftman
and Manter, 1935; Susman, 1983). However, personal
observations of the foot skeleton of an adult male bonobo, together with the interpretation of plantar pressure distributions of bonobos, point in the direction of
the cuboid-metatarsal V joint (see also D’ Août et al., in
press). In the latter, the range of motion appears to be
markedly larger than in the calcaneo-cuboid joint.
Further morphological research on ape feet should
bring more clarity.
CONCLUSIONS
Analysis of plantar pressure distributions, collected
during terrestrial locomotion of the bonobo, points to
some differences between bipedal and quadrupedal
walking. Quadrupedalism has a curved course of the
center of pressure, caused by a medial weight transfer
during mid-stance. Bipedal walking has a more irregular course of the center of pressure and is characterized by a significantly smaller contact time, according
to a smaller step length at higher frequency. Additionally, the feet are more plantar-positioned to maintain
We thank the Royal Zoological Society of Antwerp
and the Planckendael staff for allowing us to work
with the bonobos, and in particular the bonobo keepers
for their cooperation. Dr. Clark S. Larsen and two
anonymous reviewers provided constructive comments on an earlier version of the manuscript. This
research was supported by FWO-Flanders (project
G.0209.99, to P.A., D.D.C., and L.V.E.) and by the
University of Antwerp (Dehousse mandate to E.V.).
We also thank the Flemish Government for structural
support throught the Centre for Research and Conservation (Royal Zoological Society of Antwerp).
LITERATURE CITED
Aerts P, Declerq D. 1993. Deformation characteristics of the heel
region of the shod foot during a simulated heel strike: the effect
of varying midsole hardness. J Sport Sci 11:449 – 461.
Aerts P, Van Damme R, Van Elsacker L, Duchêne V. 2000.
Spatio-temporal gait characteristics of the hind-limb cycles
during voluntary bipedal and quadrupedal walking in bonobos
(Pan paniscus). Am J Phys Anthropol 111:503–517.
Aiello L, Dean C. 1996. An introduction to human evolutionary
anatomy. London: Academic Press.
Bauer HR. 1977. Chimpanzee bipedal locomotion in the Gombe
National Park, East Africa. Primates 18:913–921.
Benton MJ. 1997. Vertebrate palaeontology, 2nd ed. London:
Chapman and Hall.
Carlet G. 1872. Sur la locomotion humaine. Ann Sci Nat Ser
5:1–92.
Chen F-C, Li W-H. 2001. Genomic divergences between humans
and other hominoids and the effective population size of the
common ancestor of humans and chimpanzees. Am J Hum
Genet 68:444 – 456.
Coolidge HJ. 1933. Pan paniscus: pygmy chimpanzee from south
of the Congo River. Am J Phys Anthropol 18:1–57.
D’Août K, Aerts P, De Clercq D, Schoonaert K, Vereecke E, Van
Elsacker L. 2001. Studying bonobo (Pan paniscus) locomotion
using an integrated setup in a zoo environment: preliminary
results. Primatology 4:191–206.
D’Août K, Aerts P, De Clercq D, De Meester K, Van Elsacker L. In
press. Segment and joint angles of the hindlimb during bipedal
and quadrupedal walking of the bonobo (Pan paniscus). Am J
Phys Anthropol 119:37–51.
De Clercq D, Aerts P, Kunnen M. 1994. The mechanical characteristics of the human heel pad during foot strike in running: an
in vivo cineradiographic study. J Biomech 27:10:1213–1222.
Doran DM. 1989. Chimpanzee and pygmy chimpanzee positional
behavior: the influence of environment, body size, morphology,
and ontogeny on locomotion and posture. Ph.D. thesis, State
University of New York, Stony Brook.
Elftman H. 1944. The bipedal walking of the chimpanzee. Mammalogy 25:67–71.
Elftman H, Manter J. 1935. Chimpanzee and human feet in
bipedal walking. Am J Phys Anthropol 20:69 –79.
Fleagle JG. 1979. Primate positional behavior and anatomy: naturalistic and experimental approaches. In: Morbeck ME,
Preuschoft H, Gomberg N, editors. Environment, behavior and
PLANTAR PRESSURE OF BONOBOS
morphology: dynamic interactions in primates. New York:
Gustav Fischer. p 313–325.
Fleagle JG. 1999. Primate adaptation and evolution. New York:
Academic Press.
Fleagle JG, Stern JT, Jungers WL, Susman RL, Vangor AK,
Wells JP. 1981. Climbing: a biomechanical link with brachiation and with bipedalism. Symp Zool Soc Lond 48:359 –375.
Gebo DL. 1992. Plantigrady and foot adaptation in African apes:
implications for hominid origins. Am J Phys Anthropol 89:29–58.
Gebo DL. 1993. A reply to Dr. Meldrum. Am J Phys Anthropol
91:382–385.
Hildebrand M. 1967. Symmetrical gaits of primates. Am J Phys
Anthropol 26:119 –130.
Inman VT, Ralston HJ, Todd F. 1981. Human walking, Baltimore: Williams & Wilkins.
Ishida H, Kumakura H, Kondo S. 1985. Primate bipedalism and
quadrupedalism: comparative electromyography. In: Kondo S,
Ishida H, Kimura T, Okada M, Yamazaki N, Prost JH, editors.
Primate morphophysiology, locomotor analysis and human bipedalism. Tokyo: University of Tokyo Press. p 59 –79.
Jablonski NG, Chaplin G. 1993. Origin of habitual terrestrial
bipedalism in the ancestor of the Hominidae. J Hum Evol
24:259 –280.
Jenkins FA. 1972. Chimpanzee bipedalism: cineradiographic
analysis and implications for the evolution of gait. Science
178:877– 879.
Kano T. 1992. The last ape: pygmy chimpanzee behavior and
ecology. Stanford, CA: Stanford University Press. p 123–125.
Keith A. 1929. The history of the human foot and its bearing on
orthopaedic practice. J Bone Joint Surg 11:10 –32.
Kerr BA, Beauchamp L, Fisher V, Neil R. 1983. Footstrike patterns in distance running. In: Nigg B, Kerr BA, editors. Biomechanical aspects of sport shoes and playing surfaces. Calgary:
University Press. p 135–143.
Kimura T. 1985. Bipedal and quadrupedal walking of primates:
comparative dynamics. In: Kondo S, Ishida H, Kimura T,
Okada M, Yamazaki N, Prost JH, editors. Primate morphophysiology, locomotor analysis and human bipedalism. Tokyo:
University of Tokyo Press. p 81–104.
Kimura T. 1990. Voluntary bipedal walking of infant chimpanzees. In: Jouffroy FK, Stack MH, Niemitz C, editors. Gravity,
posture and locomotion in primates. Florence: II Sedicesimo. p
237–251.
Kimura T. 1996. Centre of gravity of the body during the ontogeny of chimpanzee bipedal walking. Folia Primatol (Basel) 66:
126 –136.
Kimura T, Okada M, Ishida H. 1977. Dynamics of primate bipedal
walking as viewed from the force of foot. Primates 18:137–147.
Kimura T, Okada M, Yamazaki N, Ishida H. 1983. Speed of the
bipedal gaits of man and nonhuman primates. Ann Sci Nat Zool
Paris 5:145–158.
Langdon JH. 1986. Functional morphology of the Miocene hominoid foot. New York: Karger.
Li Y, Crompton RH, Alexander RMN, Günther MM, Wang WJ.
1996. Characteristics of ground reaction forces in normal and
chimpanzee-like bipedal walking by humans. Folia Primatol
(Basel) 66:137–159.
Marey M. 1873. De la locomotion terrestre chez les bipedes et
quadrupedes. J Anat Physiol 9:42.
McHenry HM. 1984. The common ancestor. A study of the postcranium of Pan paniscus, Australopithecus and other hominoids. In:
Susman RL, editor. The pygmy chimpanzee. Evolutionary biology
and behavior. New York: Plenum Press. p 201–224.
McHenry HM, Corruccini RS. 1981. Pan paniscus and human
evolution. Am J Phys Anthropol 54:355–367.
Meldrum DJ. 1991. Kinematics of the Cercopithecine foot on
arboreal and terrestrial substrates with implications for the
interpretation of hominid terrestrial adaptations. Am J Phys
Anthropol 84:273–290.
Meldrum DJ. 1993. On plantigrady and quadrupedalism. Am J
Phys Anthropol 91:379 –385.
Morton DJ. 1922. Evolution of the human foot I. Am J Phys
Anthropol 5:305–336.
383
Morton DJ. 1924. Evolution of the human foot II. Am J Phys
Anthropol 7:1–52.
Okada M. 1985. Primate bipedal walking: coparative kinematics.
In: Kondo S, Ishida H, Kimura T, Okada M, Yamazaki N, Prost
JH, editors. Primate morphophysiology, locomotor analysis and
human bipedalism. Tokyo: University of Tokyo Press. p 47–58.
Perry J. 1992. Gait analysis: normal and pathological function.
Thorofare, NJ: Slack.
Prost JH. 1980. Origin of bipedalism. Am J Phys Anthropol 52:
175–189.
Reynolds TR. 1985. Stresses on the limbs of quadrupedals primates. Am J Phys Anthropol 67:351–362.
Rose MD. 1991. The process of bipedalization in hominids. In:
Coppens Y, Senut B, editors. Origine(s) de la bipédie chez les
hominidés (Cahiers de Paléanthropologie). Paris: Editions du
CNRS. p 37– 48.
Rosenbaum D, Hautman S, Gold M, Claes L. 1994. Effects of
walking speed on plantar pressure patterns and hindfoot angular motion. Gait Posture 2:191–197.
Schmitt D, Larson SG. 1995. Heel contact as a function of substrate
type and speed in primates. Am J Phys Anthropol 96:39–50.
Senut B. 1992. New ideas on the origins of hominid locomotion. In:
Nishida T, McGrew WC, Marker P, Pickford M, de Waal FBM,
editors. Topics in primatology. Volume I: human origins. Tokyo:
University of Tokyo Press. p 393– 407.
Susman RL. 1983. Evolution of the human foot: evidence from
Plio-Pleistocene hominids. Foot Ankle 3:365–376.
Susman RL. 1984. The locomotor behavior of Pan paniscus in the
Lomako forest. In: Susman RL, editor. The pygmy chimpanzee.
Evolutionary biology and behavior. New York: Plenum. p 369 –
393.
Susman RL, Badrian NL, Badrian AJ. 1980. Locomotor behavior
of Pan paniscus in Zaire. Am J Phys Anthropol 53:69 – 80.
Susman RL, Stern JT Jr. 1991. Locomotor behavior of early hominids: epistemology and fossil evidence. In: Coppens Y, Senut B,
editors. Origine(s) de la bipédie chez les hominidés (Cahiers de
Paléanthropologie). Paris: Editions du CNRS. p 121–131.
Tuttle RH. 1970. Postural, propulsive and prehensile capabilities
in the cheiridia of chimpanzees and other great apes. Chimpanzee 2:167–253.
Van Elsacker L, Claes G, Melens W, Struyf K, Vervaecke H, Walraven V. 1993. New outdoor exhibit for a bonobo group at Planckendael: design and introduction procedures. In: Daman FJ, editor.
Bonobo tidings, jubilee volume on the occasion of the 150th anniversary of the Royal Zoological Society of Antwerp. Antwerp:
Royal Zoological Society of Antwerp. p 35– 47.
Whittle MW. 1996. Basic sciences. Gait analysis, an introduction.
2nd ed. Oxford: Butterworth-Heinemann.
Wood BA. 1992. Evolution of australopithecines. In: Jones S,
Martin R, Pilbeam D, editors. The Cambridge encyclopedia of
human evolution. Cambridge: Cambridge University Press. p
231–240.
Wunderlich RE. 1999. Pedal form and plantar pressure distribution in anthropoid primates. Ph.D. thesis. Ann Arbor, MI: Bell
& Howell (UMI Dissertation Services).
Wunderlich RE, Ford KR. 2000. Plantar pressure distribution
during bipedal and quadrupedal walking in the chimpanzee
(Pan troglodytes). Proceedings of EMED Scientific Meeting,
2– 6 August 2000. p 19.
Zihlman AL. 1984. Body build and tissue composition in Pan paniscus and Pan troglodytes, with comparison to other hominoids. In:
Susman RL, editor. The pygmy chimpanzee. Evolutionary biology
and behavior. New York: Plenum Press. p 179–200.
Zihlman AL. 1992. The emergence of human locomotion: the
evolutionary background and environmental context. In:
Nishida T, McGrew WC, Marker P, Pickford M, de Waal FBM,
editors. Topics in primatology. Volume 1: human origins. Tokyo: University of Tokyo Press. p 409 – 442.
Zihlman AL, Cramer DL. 1978. Skeletal differences between
pygmy (Pan paniscus) and common chimpanzees (Pan troglodytes). Folia Primatol (BaseI) 29:86 –94.
Zihlman AL, Cronin JE, Cramer DL, Sarich VM. 1978. Pygmy
chimpanzee as a possible prototype for the common ancestor of
humans, chimpanzees and gorillas. Nature 275:744 –746.
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locomotive, distributions, plantar, pan, pressure, paniscus, dynamics, terrestrial, bonobos
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