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Brief communication Dynamic plantar pressure distribution during locomotion in Japanese macaques (Macaca fuscata).

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:149–156 (2010)
Brief Communication: Dynamic Plantar Pressure
Distribution during Locomotion in Japanese Macaques
(Macaca fuscata)
Eishi Hirasaki,* Yasuo Higurashi, and Hiroo Kumakura
Laboratory of Biological Anthropology, Graduate School of Human Sciences, Osaka University, Suita,
Osaka 565-0871, Japan
KEY WORDS
foot function; bipedal walking; quadrupedal walking; kinetics
ABSTRACT
To better place the form and motion of
the human foot in an evolutionary context, understanding
how foot motions change when quadrupeds walk bipedally can be informative. For this purpose, we compared
the pressures beneath the foot during bipedal and quadrupedal walking in Japanese macaques (Macaca fuscata).
The pressure at nine plantar regions was recorded using
a pressure mat (120 Hz), while the animals walked on a
level walkway at their preferred speeds. The results
revealed substantial differences in foot use between the
two modes of locomotion, and some features observed during bipedal walking resembled human gait, such as the
medial transfer of the center of pressure (COP), abrupt
declines in forefoot pressures, and the increased pressure
beneath the hallux, all occurring during the late-stance
phase. In particular, the medial transfer of the COP,
which is also observed in bonobos (Vereecke et al.: Am J
Phys Anthropol 120 (2003) 373–383), was due to a biomechanical requirement for a hind limb dominant gait, such
as bipedal walking. Features shared by bipedal and quadrupedal locomotion that were quite different from human
locomotion were also observed: the heel never contacted
the ground, a foot longitudinal arch was absent, the hallux was widely abducted, and the functional axis was on
the third digit, not the second. Am J Phys Anthropol
142:149–156, 2010. V 2009 Wiley-Liss, Inc.
Obligate bipedal locomotion is a feature that separates
humans from other primates. To better understand the
mechanics of human bipedal locomotion, many experimental studies have examined bipedal and quadrupedal
walking in nonhuman primates (e.g., Jenkins, 1972;
Ishida et al., 1974; Kimura et al., 1979; Yamazaki et al.,
1979; Stern and Susman, 1981; Shapiro and Jungers,
1988; Aerts et al., 2000; D’Août et al., 2004). The biomechanical conditions required for the evolution of this
type of gait, however, are not fully understood, partly
because quantitative data are lacking on the motion of
the foot during locomotion. Because the foot performs a
pivotal role in the interaction between the body and the
substrate during locomotion (Sigmon and Farslow, 1986),
studies have focused on the morphology and function of
the foot, and a great deal of information has accumulated from studies on primate feet and fossil evidence
from early hominids (e.g., Susman, 1983; Lewis, 1989;
Gebo, 1993a; Vereecke et al., 2005a). Foot kinematics
and kinetics during primate locomotion have also been
studied, based mostly on qualitative observations
(Elftman and Manter, 1935; Okada, 1985; Meldrum,
1991, 1993; Gebo, 1992, 1993a,b; Schmitt and Larson,
1995), and they have contributed to understand the evolution of human locomotor strategies (Wunderlich, 1999).
Quantitative comparisons of foot motion during bipedal
and quadrupedal walking, however, are relatively scarce,
with the exceptions of the studies by Wunderlich (1999,
2003) and Vereecke et al. (2003). To better understand
the form and motion of the human foot in an evolutionary context, knowing how foot motions change when
quadrupeds walk bipedally can be informative, because
that is what happened when our ancestors stood up on
the ground or when early hominoids stood up on a
branch (Crompton et al., 2003, 2008).
For this study, we obtained quantitative data on the
pressure beneath the foot during quadrupedal and
bipedal walking in Japanese macaques, emphasizing the
differences between the two modes of locomotion.
Although African apes may be more appropriate subjects
for studying the evolution of bipedalism (Vereecke et al.,
2003, 2004, 2005b), we reduced the effects of synapomorphy by using macaques, which are phylogenetically farther from humans than African apes. Consequently, any
humanlike features found in the bipedal gait of macaques can be more plausibly attributed to the biomechanical requirements of bipedal walking rather than to
synapomorphy (Hirasaki et al., 2004). Therefore, we
measured foot pressures in macaques during bipedal
walking and examined how they differed from those during quadrupedal walking.
C 2009
V
WILEY-LISS, INC.
C
Grant sponsor: Japan Society for the Promotion of Science; Grant
number: 14704005.
*Correspondence to: Eishi Hirasaki, Laboratory of Biological
Anthropology, Graduate School of Human Sciences, Osaka University 1-2 Yamadaoka, Suita, Osaka 565-0871, Japan.
E-mail: hirasaki@hus.osaka-u.ac.jp
Received 19 February 2009; accepted 28 October 2009
DOI 10.1002/ajpa.21240
Published online 21 December 2009 in Wiley InterScience
(www.interscience.wiley.com).
150
E. HIRASAKI ET AL.
TABLE 1. Gait parameters during the quadrupedal and bipedal sequences, in which pressure data were collected
Quadrupedal (n 5 13)
Bipedal (n 5 14)
Significance
Walking speed (km/h)
Stride length (m)
Step frequency (Hz)
Contact duration (s)
Duty factor (%)
2.79 (60.17)
2.91 (60.14)
n.s
0.73 (60.03)
0.68 (60.03)
P \ 0.001
2.11 (60.16)
2.39 (60.10)
P \ 0.001
0.60 (60.04)
0.54 (60.05)
P \ 0.01
63.7 (62.5)
64.1 (62.3)
n.s.
Values are the mean 6 SD. Student’s t test was used to compare the results between quadrupedal and bipedal walking.
During bipedal walking, only two limbs support the
body, which is reflected in many aspects of the plantar
pressure profiles. We predicted the following. First, the
pressures would be substantially higher during bipedal
walking than during quadrupedal walking; the higher
step frequency of bipedal walking (Kimura, 1985; Aerts
et al., 2000; Hirasaki and Kumakura, 2004) would also
increase plantar pressures. Second, the hallux would be
abducted more during bipedal walking to provide more
stability. Third, the center of pressure (COP) would
mediolaterally deviate more during bipedal walking than
during quadrupedal walking, because the upper part of
the body is supported only by one hind limb during the
single-limb support phase of bipedal walking. In particular, the trunk moves laterally toward the side of the
swinging hind limb at the end of the stance phase.
Therefore, our third prediction can be rephrased as follows: the COP would deviate more medially at the end of
stance phase during bipedal walking than during quadrupedal walking.
MATERIALS AND METHODS
We studied two adult Japanese macaques (Macaca
fuscata), a 10.6-kg, 16-year-old male, and a 4.7-kg,
11-year-old, female. During bipedal and quadrupedal
walking on the floor, the foot-pressure distribution was
recorded using a sensor sheet (Big-mat 1/4, 22 3
24 cm2, 5-mm resolution; distributed in Japan by Nitta
in cooperation with Tekscan, Boston, MA) at a sampling
frequency of 120 Hz. The sheet was sufficiently large
(440 3 480 mm2) to accommodate the feet of the macaques (length, L: L 5 157 mm and L 5 138 mm). To
examine steady-state locomotion, the sensor sheet was
set at the center of the 7-m walkway. The macaques
walked at their preferred walking speeds. Two video
cameras were set perpendicular to the walkway: a distant one was used to measure walking speed and a
close one to capture foot images. A third video camera
was placed at the end of walkway to monitor the progression of the macaques along the long axis of the
walkway.
We analyzed only sequences in which at least one complete foot-pressure profile was recorded, and the animal
walked parallel to the long axis of the walkway at a
steady speed. For each foot-pressure image, the COP
was estimated in the same manner as for estimating the
center of gravity (Goldstein, 1980). Functional foot
length was defined as the length from the proximal-most
point of the contact area of the foot to the distal-most
point of the third digit (Vereecke et al., 2003). The footprogression angle, which was defined as the angle
between the lines used to measure functional foot length
and the direction of progress (i.e., the long axis of the
walkway), was calculated to estimate out-toeing. Hallux
abduction was defined as the angle between the long
axis of the hallux and the line representing the functional foot length defined earlier. Nine foot regions were
American Journal of Physical Anthropology
defined based on the functional morphology of the macaque foot: the tarsal area, medial (second and third) metatarsal shafts (hereafter, referred to as the ‘‘medial metatarsals’’), lateral (fourth and fifth) metatarsal shafts
(‘‘lateral metatarsals’’), first metatarsophalangeal (MP)
joint (MPJ I), medial (second and third) MP joints (MPJ
II, III), lateral (fourth and fifth) MP joints (MPJ IV, V),
hallux, medial (second and third) digits (Digits II, III),
and lateral (fourth and fifth) digits (Digits IV, V). The
second and third and the fourth and fifth MP joints were
analyzed as the ‘‘medial’’ and ‘‘lateral’’ MP joints, respectively, because the resolution of the system (5 mm) was
insufficient to define areas for each metatarsal head
accurately. The same was true for the digits. In each of
the nine regions, the 1-cm2 area with the highest pressure throughout the stance phase was chosen, and the
changes in pressure in each regional peak pressure area
were recorded. The palmar pressures were also recorded,
but it will not be discussed here as they are beyond the
scope of this study.
Although our animals walked at their preferred walking speed, which ranged from 1.3 to 4.3 km/h, we
selected narrow and similar speed ranges (2.5–3.1 km/h
for quadrupedalism and 2.6–3.1 km/h for bipedalism)
for the analyses in this study to avoid the confounding
effects of walking speed on the pressure profiles. However, we plan to address the effects of walking speed in
future studies, as it has been reported that speed influences the plantar (and palmar) pressures (Rosenbaum
et al., 1994; Vereecke et al., 2005b; Patel and Wunderlich, 2008). The experiment was approved by the Institutional Animal Care and Use Committee of Osaka
University.
RESULTS
Although the subjects walked at similar speeds during
quadrupedal (2.79 km/h) and bipedal (2.91 km/h) walking (Table 1), the step frequency and stride length differed between the two modes of locomotion. During
bipedal walking, the strides were shorter and the step
frequencies were higher than during quadrupedal walking. The absolute contact durations were shorter in
bipedal walking than in quadrupedal walking, but no
significant difference was found in the duty factors
(Table 1). These tendencies were consistent with previous studies of Japanese macaques (Kimura, 1985; Hirasaki and Kumakura, 2004) and bonobos (Aerts et al.,
2000).
Foot pressure profile during quadrupedal walking
The foot-pressure profile analysis showed that the first
contact during quadrupedal walking was typically made
by the tarsal area close to the calcaneocuboid joint
(Fig. 1a). The heel never touched down throughout the
stance phase, as indicated by the fact that the functional
foot length was significantly shorter (81.4%) than the
actual foot length (Table 2). Because the toe tips were in
151
PLANTAR PRESSURE DISTRIBUTION IN MACACA FUSCATA
Fig. 1. Plantar pressure profiles during quadrupedal and bipedal walking in Japanese macaques (Macaca fuscata). (a) Typical
pressure profiles at five specific times of the stance phase during quadrupedal and bipedal walking, respectively. The highest pressure is in red and the lowest in dark blue. The periods expressed as the percentage of stance phase duration are shown below each
panel. To help clarify which part of the foot was in contact at each instant, the contour of the entire contact area of the foot during
the stance phase is superimposed. (b) The typical foot posture during quadrupedal walking. (c) Typical pressure profiles during
bipedal walking. During bipedal walking, initial contact was made by the lateral forefoot close to the fifth metatarsal head, whereas
the tarsal part touched down first during quadrupedal walking. (d) The typical foot posture during bipedal walking. (e) Typical trajectory of the center of pressure (COP) during quadrupedal walking. The trajectory was relatively straight. (f) A case in which the
hallux supported more weight during quadrupedal walking. (g) A typical trajectory of the COP during bipedal walking. The COP
shifted medially at the level of the metatarsal heads.
TABLE 2. Functional foot length, foot-progression angle, and hallux abduction during locomotion
Quadrupedal (n 5 13)
Bipedal (n 5 14)
Significance
Functional foot length (%)
Foot-progression angle (8)
Hallux abduction (8)
81.6 6 2.7
83.1 6 3.9
n.s.
5.4 6 6.4
9.0 6 7.5
n.s.
44.6 6 4.6
53.5 6 9.7
P \ 0.01
Values are the mean 6 SD. Student’s t test was used to compare the results between quadrupedal and bipedal walking.
Fig. 2. Pressures on each area of the foot during (a) quadrupedal and (b) bipedal walking. An important difference between the
two modes of locomotion was that the values were greater for the medial digits (broken red line) and metatarsal heads (solid red
line) than for the lateral digits (broken green line) and metatarsal heads (solid green line) during bipedal walking, especially in the
later stance phase, whereas no such tendency was observed during quadrupedal walking. Another difference was in the use of the
hallux; the pressure at the hallux (broken blue line) and first metatarsal head (solid blue line) peaked later in the stance phase during bipedal walking and in the mid-stance phase during quadrupedal walking.
American Journal of Physical Anthropology
152
E. HIRASAKI ET AL.
Fig. 4. The mediolateral ratio of plantar pressures. The ratio was calculated as the sum of the pressures for the medial
(second and third) metatarsals, medial MP joints, and medial
digits, divided by the sum of the pressures for the lateral
(fourth and fifth) metatarsals, lateral MP joints, and lateral digits. The solid and broken lines represent bipedal and quadrupedal gait, respectively.
Fig. 3. The relative contact timing and duration for the nine
foot regions expressed as a percent of the total stance phase duration during (a) quadrupedal and (b) bipedal locomotion. M,
metatarsals 5 medial metatarsal shafts; L, metatarsals 5 lateral metatarsal shafts; MPJ I 5 first metatarsophalangeal (MP)
joints; MPJ II, III 5 second and third MP joints; MPJ IV, V 5
fourth and fifth MP joints; Digits II, III 5 second and third digits; Digits IV, V 5 fourth and fifth digits. Blackened areas indicate that the foot region was in contact with the ground in more
than 75% of the measured steps; dark gray areas indicate frequent, but less predictable contact (50–75%); light gray areas
indicate contact of the foot region occurring in between 25 and
50% of the steps.
contact with the ground, and digits were not curled very
much (Fig. 1b), unlike in the case of bonobos (Vereecke
et al., 2003), the shorter functional foot length indicates
that the heel was elevated.
The greatest pressure during the early stance phase
was observed in the tarsal region close to the calcaneocuboid joint (Figs. 1a,e and 2a, black line). Then, the COP
progressed toward the third metatarsal head at the early
stance phase in a relatively straight trajectory (Fig. 1e).
At the mid-stance phase, the tarsal and metatarsal
regions of the foot were elevated (Figs. 1a and 3a), and
the pressure was greatest near the second to fifth metatarsal heads (Figs. 1a,e and 2a, solid green and red
lines), although the values were slightly larger at the
lateral metatarsal heads (green line) than the medial
ones (red line). Next, the COP shifted medially slightly,
but the pressures under the lateral regions of the foot
were larger than those under the medial regions
throughout the stance phase (Fig. 4, broken line). The
COP shifted farther to the third digit, which left the substrate last, suggesting that the functional axis of the
macaque foot is aligned with the third digit. The hallux,
which left the ground earlier than the other digits, and
the first metatarsal head had their peak pressures in the
early stance phase (Fig. 2a, solid and broken blue lines,
respectively).
American Journal of Physical Anthropology
A different pattern in which the hallux touched
down first, as in the case of bonobo bipedal and quadrupedal walking and gibbon bipedal walking (Vereecke
et al., 2003, 2005b), was also found in 30–40% of the
walking sequences collected. In most cases, the initial
touch was light, but occasionally the hallux supported
more weight during the early stance phase, resulting
in a V-shaped trajectory and medial deviation of the
COP (Fig. 1f). This was observed in both of the study
subjects.
Foot-pressure profile during bipedal walking
During bipedal walking, the initial contact was
almost always made by the lateral forefoot close to the
fifth metatarsal head (Figs. 1c and 3b), suggesting that
the foot was in an inverted position. This was consistent with Okada’s (1985) observation in the same species. Then, the foot was everted gradually. The COP
first traveled backward to the tarsal area, although the
heel never touched the floor (Fig. 1d), as indicated by a
functional foot length that was shorter than the actual
foot length (83.1%, Table 2). This value was similar to
that during quadrupedal walking (81.4%), despite the
foot supporting substantially more weight during
bipedal walking than during quadrupedal walking. The
greater weight supported resulted in higher peak pressures; the peak pressure for each foot region during
bipedal walking was more than twice that during quadrupedal walking (Fig. 2, Table 3). The greatest pressure
during the early stance phase was observed near the
calcaneocuboid joint (Figs. 1c, 1g, and 2b, black line),
as in quadrupedal walking. Unlike the roll-off pattern
in a quadrupedal gait, however, the tarsal and metatarsal regions of the foot remained in contact with the
ground until later in the stance phase (Fig. 3). This is
seen clearly in the COP fore-aft movements; the COP
during bipedal walking stayed proximally much longer
(until ca. 30% of the stance phase, Fig. 5) and then progressed anteriorly during the flat foot and mid-stance
phases (Fig. 1g). This may have resulted from the
difference in trunk posture. Because the center of the
PLANTAR PRESSURE DISTRIBUTION IN MACACA FUSCATA
153
TABLE 3. The maximum pressure for each foot region
Quadrupedal
(kPa) (n 5 13)
Tarsal area
M. metatarsals
L. metatarsals
MPJ I
MPJ II, III
MPJ IV, V
Hallux
Digits II, III
Digits IV, V
49.3
21.3
29.0
52.5
48.5
56.0
34.8
33.2
32.6
6
6
6
6
6
6
6
6
6
11.5
3.5
12.2
27.7
14.9
19.8
19.4
13.3
18.2
Bipedal
(kPa) (n 5 14)
102.5
52.2
55.0
85.1
98.1
69.9
75.2
78.8
48.2
6
6
6
6
6
6
6
6
6
16.4
25.6
7.5
53.5
32.4
21.7
49.9
5.4
9.3
See text and Fig. 3 for the abbreviations.
body mass is located in the lumbar region of the trunk,
its position relative to the feet is more forward in pronograde postures than in orthograde postures, inducing
rapid forward transfer of the COP during quadrupedal
walking. In contrast, when walking bipedally, the center of mass is at the rear of the foot during the early
half of the stance phase, keeping the COP in the proximal regions of the foot.
Occasionally, the hallux touched down first, as in the
case of quadrupedal walking. However, this was less frequent than during quadrupedal walking (\15%), and the
touch appeared to be light; this was followed immediately by substantial touchdown of the tarsal region close
to the calcaneocuboid joint. The V-shaped trajectory of
the COP was found in one walking sequence only. In the
other case, the initial contact by the hallux was not
reflected in the trajectory of the COP because of the
small values and short duration.
At 60% of the stance phase, the COP started to shift
medially, as clearly shown in Figure 4. Because no significant difference was seen in the pressures between
the medial and lateral metatarsal regions (Fig. 2, brown
and orange lines, respectively), the medial transfer of
the COP occurred at the level of the metatarsal heads
(Fig. 2). At toe-off, the COP shifted laterally (Fig. 4) and
the third digit left the substrate last (Fig. 1g). Abrupt
declines occurred in the digit pressures at the end of the
stance phase, which resembled the human gait (Fig. 2b,
green and red-broken lines).
The pressures at the first MP joint (Fig. 2b, solid blue
line) and hallux (broken blue line) peaked late in the
stance phase, and their magnitudes were similar to that
of the lateral MP joints, suggesting that the big toe
played a more important role during bipedal walking
than during quadrupedal walking. Nevertheless, as in
the case of quadrupedal walking, the hallux left the
ground before the other digits due to its abducted position. The hallux was abducted substantially during both
bipedal and quadrupedal walking, and abduction was
more prominent during bipedal walking than during
quadrupedal walking (Table 2, P \ 0.05).
The foot-progression angle measurements revealed
that the foot was out-toed slightly more during bipedal
walking than during quadrupedal walking, although the
difference was not significant due to the large variation
(Table 2). In addition, the direction of walking was
defined as the long axis of the walkway. Although we
removed the sequences in which the animals did not
walk parallel to the walkway, this definition might have
reduced the reliability of the foot-progression angle
values.
Fig. 5. Fore-aft movement of the COP is represented as the
relative distance from the tip of the third digit, and is plotted
against time expressed as a percentage of the stance phase. The
solid and broken lines represent bipedal and quadrupedal gaits,
respectively. The COP in bipedal walking traveled backward
first and stayed close to the tarsal area for much longer than
during quadrupedal walking.
In all the analyzed sequences of both bipedal and
quadrupedal walking, the medial metatarsal area was in
contact with the ground (Figs. 1 and 2), suggesting that
no longitudinal foot arch exists in the macaque foot.
DISCUSSION
The main finding of this study was that Japanese macaques use their feet very differently in bipedal and quadrupedal locomotion. As expected, the pressures were
much greater during bipedal walking than during quadrupedal walking (Fig. 2 and Table 3). This was not surprising, as only two hind limbs support the body weight
during bipedal walking, whereas all four limbs do so
during quadrupedal walking. However, because the hind
limbs of the Japanese macaque support more weight
than the forelimbs during quadrupedal walking
(Kimura, 1985; Hirasaki and Matano, 1996), the
observed peak values of bipedal walking, which were
more than twice larger than those of quadrupedal walking, seemed to be too great. Shorter contact durations
(Table 1) during bipedal walking likely increased the
peak values.
The trajectory of the COP also differed between the
two modes of locomotion. During quadrupedal walking,
the COP traveled in a relatively straight line forward
from the tarsal area to the third or fourth digit, whereas
during bipedal walking, it traveled backward from the
lateral metatarsal to the tarsal area and then moved forward and medially across the metatarsal heads. The
later part of this motion (i.e., the medial transfer)
resembled the human COP trajectory. In humans, the
COP transfers medially to the second MP joint at the
end of the stance phase (e.g., Barnett, 1956). Because
this pattern was also observed in Japanese macaques,
which are phylogenetically distant from humans, it sugAmerican Journal of Physical Anthropology
154
E. HIRASAKI ET AL.
gests that the medial transfer at the end of the stance
phase results from the biomechanical requirements of
bipedal walking; in bipedal walking, the upper part of
the body is supported only by one hind limb during single-limb support phase and moves laterally onto the
other hind limb at the end of the stance phase. With this
lateral movement of body mass and probably because of
the slightly more out-toed feet, the COP is transferred
medially at the end of the stance phase. In contrast, during quadrupedal walking, the lateral movement of the
body due to hind limb alteration is likely attenuated by
forelimb support, resulting in the relatively straight trajectory of the COP. This is consistent with Kimura’s
(1985) finding that the lateral component of the floor
reaction force is greater during bipedal walking than
during quadrupedal walking.
In bonobos, unlike in Japanese macaques, quadrupedal walking is most often associated with a curved COP
trajectory (Vereecke et al., 2003); this results in the functional foot axis running through the second digit. We attribute the difference between Japanese macaques and
bonobos to the difference between a semipalmigrade
quadrupedal gait and knuckle walking; during knuckle
walking, the forelimbs support a much smaller proportion of the body weight compared to the semipalmigrade/
palmigrade quadrupedal gait (Kimura et al., 1979;
Kimura, 1985; Demes et al., 1994). The forelimb support
in knuckle walking may not be sufficient to attenuate
the lateral movement of the body, which results in the
medial shift of the COP trajectory at the late-stance
phase.
The difference in the initial contact between the two
modes of locomotion suggests that the foot was more outtoed, inverted, and down-toed (i.e., the toes are lower
than the heel) when touching down in bipedal walking
than in quadrupedal walking. As shown in Table 1, the
foot was slightly more out-toed during bipedal walking,
although the difference was not significant due to the
large standard deviations and a small sample size. The
out-toed, inverted foot at touchdown may result from the
externally rotated thigh during bipedal walking; this
needs to be confirmed by kinematic data, which is outside the scope of this paper. The down-toed foot postures
may be partly attributable to the shorter stride length
during bipedal walking compared to quadrupedal walking (Table 1); with a shorter stride, the hind limbs are
not protracted as much, resulting in relatively downward
foot postures, given a constant talocrural joint angle.
Another difference between the two modes of locomotion was in the use of the hallux. The maximum pressures at the hallux and first MP joint were observed at
the late-stance phase during bipedal walking and the
mid-stance phase of quadrupedal walking (Fig. 2). This
seems unusual, because the hallux was abducted more
during bipedal walking. This may have occurred partly
because the COP progressed more slowly during bipedal
walking than during quadrupedal walking (Figs. 3 and
5). In addition, out-toeing may increase the importance
of the hallux for generating propulsive force in bipedal
walking. The important role of the hallux in the latestance phase during bipedal walking again recalls
human foot motions.
The hallux of the Japanese macaques often touched
down first during both modes of locomotion, although
this was less frequent during bipedal walking. Initial
hallux contact is also observed in sifakas (Wunderlich
and Schaum, 2007) and gibbons (Vereecke et al., 2005b)
American Journal of Physical Anthropology
and occasionally in bonobos (Vereecke et al., 2003). Vereecke et al. (2005b) postulated that this pattern was due
to the arboreally adapted foot anatomy of apes (widely
abducted hallux, especially in gibbons). This concurs
with Okada’s (1985) report that hallucial plantar-flexion
before touchdown is frequently observed in arboreal spider monkeys, whereas terrestrial baboons do not show
it. In contrast, in humans, the hallux is usually dorsiflexed before touchdown. Okada (1985) argued that the
hallucial dorsiflexion in humans evolved to enhance the
foot arch and to strain the sole before touchdown. If this
is true, bipedal walking of the Japanese macaque, in
which initial hallucial contact is infrequent, could be an
adaptation to terrestrial locomotion, although this is
speculative and more information is necessary.
Another important point is the abrupt decline in pressures during the late-stance phase in bipedal walking
(Fig. 2b). This was not observed during quadrupedal
walking by Japanese macaques (Fig. 2a) and is also
absent during ape locomotion (Vereecke et al., 2003,
2005b). The smoother declines during quadrupedal walking are thought to result from the forelimb support,
which reduces the hind limb load at the end of the
stance phase. The abrupt decline in the pressures
observed in the bipedal walking of Japanese macaques
resembles the human gait pattern. Nevertheless,
although the shape is similar, the magnitude may be
smaller, because the floor reaction force data (Ishida et
al., 1974) do not suggest a strong push-off by the toes at
the end of the stance phase. More detailed kinematic
data need to be collected simultaneously with pressure
data in future studies.
The two modes of locomotion showed several shared
features. During both bipedal and quadrupedal walking,
the Japanese macaques never touched their heel down.
They appeared to walk with terrestrial semiplantigrade
foot postures (Gebo, 1993a, b). The flexibility at the tarsometatarsal or calcaneocuboid joint (the midtarsal
break) likely makes this foot posture possible (Hirasaki
and Kumakura, 2003). Vereecke et al. (2003, 2004,
2005b) reported that the heel contacts the ground during
both bipedal and quadrupedal walking in bonobos and
during bipedal walking in gibbons, although a heelstrike comparable to human gait was observed only in
bonobos. In gibbons, the heel contacts the substrate at
mid-stance. On the basis of their results, Vereecke et al.
(2005b) suggested that heel-strike is a synapomorphy of
the great apes. In our experiments, the heel of the macaques was elevated throughout the stance phase. This
concurs with the well-accepted idea that heel contact is
unique to humans, apes, and atelines, although heelstrike is restricted to humans and great apes (Meldrum,
1991, 1993; Gebo, 1002, 1993a,b; Schmitt and Larson,
1995). Future additional evidence from other species
would increase the robustness of the idea that heel contact is one of the features distinguishing apes from monkeys. Bipedal and quadrupedal walking were also similar in that the third digit left the ground last. This indicates that the functional axis of the foot was aligned
with the third digit in Japanese macaques and is consistent with our morphological observations (Hirasaki and
Kumakura, in press) that the interosseous muscles of
the Japanese macaque are arranged around the third
digit. This is different from chimpanzees and bonobos, in
which the second digit leaves the ground last, showing
that the functional axis is on the second metatarsal and
digit (Wunderlich, 1999; Vereecke et al., 2003).
PLANTAR PRESSURE DISTRIBUTION IN MACACA FUSCATA
In
summary,
we
found
some
humanlike
characteristics in foot motion during bipedal walking—
the medial transfer of the COP, the increased importance
of the hallux during late-stance phase, and an abrupt
decline in pressures during late stance phase—in Japanese macaques and attributed them to the biomechanical
requirements of bipedal walking. Nevertheless, the other
features in the foot motion of the macaque during
bipedal walking differed greatly from those of humans:
the heel did not contact the ground, no foot longitudinal
arch was observed, the hallux was not aligned with the
other digits, and the functional axis was not aligned
with the second digit. Future studies should address
how these features evolved in humans.
ACKNOWLEDGMENTS
We express our gratitude to Dr. Evie E. Vereecke
(University of Liverpool), anonymous reviewers,
Associate Editor, and Editor-in-Chief for their invaluable comments and suggestions on this manuscript. We
are also grateful to Dr. Roshna Wunderlich (James
Madison University) and Dr. Kristiaan D’Août (University of Antwerp) for their thoughtful and constructive comments on the earlier versions of this manuscript.
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