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Energetic costs of bipedal and quadrupedal walking in Japanese macaques.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 124:248 –256 (2004)
Energetic Costs of Bipedal and Quadrupedal Walking in
Japanese Macaques
M. Nakatsukasa,1* N. Ogihara,1 Y. Hamada,2 Y. Goto,1 M. Yamada,1 T. Hirakawa,1 and E. Hirasaki3
1
Laboratory of Physical Anthropology, Kyoto University, Kyoto 606-8502, Japan
Primate Research Institute, Kyoto University, Aichi 484-8506, Japan
3
Department of Biological Anthropology, Osaka University, Osaka 565-0871, Japan
2
KEY WORDS
locomotor energetics; bipedalism; Macaca fuscata; respiratory physiology
ABSTRACT
We investigated the energetic costs of
quadrupedal and bipedal walking in two Japanese macaques. The subjects were engaged in traditional bipedal
performance for years, and are extremely adept bipeds.
The experiment was conducted in an airtight chamber
with a gas analyzer. The subjects walked quadrupedally
and bipedally at fixed velocities (⬍5 km/hr) on a treadmill
in the chamber for 2.5– 6 min. We estimated energy consumption from carbon dioxide (CO2) production. While
walking bipedally, energetic expenditure increased by
30% relative to quadrupedalism in one subject, and by
20% in another younger subject. Energetic costs increased
linearly with velocity in quadrupedalism and bipedalism,
with bipedal/quadrupedal ratios remaining almost constant. Our experiments were relatively short in duration,
and thus the observed locomotor costs may include presteady-state high values. However, there was no difference
in experimental duration between bipedal and quadrupe-
dal trials. Thus, the issue of steady state cannot cancel the
difference in energetic costs. Furthermore, we observed
that switching of locomotor mode (quadrupedalism to bipedalism) during a session resulted in a significant increase of CO2 production. Taylor and Rowntree ([1973]
Science 179:186 –187) noted that the energetic costs for
bipedal and quadrupedal walking were the same in chimpanzees and capuchin monkeys. Although the reason for
this inconsistency is not clear, species-specific differences
should be considered regarding bipedal locomotor energetics among nonhuman primates. Extra costs for bipedalism
may not be great in these macaques. Indeed, it is known
that suspensory locomotion in Ateles consumes 1.3–1.4
times as much energy relative to quadrupedal progression. This excess ratio surpasses the bipedal/quadrupedal
energetic ratios in these macaques. Am J Phys Anthropol
124:248 –256, 2004. © 2004 Wiley-Liss, Inc.
There is no living nonhuman primate in which bipedalism comprises a major positional component.
This poses an inherent problem in the study of human
bipedal adaptations through cross-species comparative methods. Living humans are highly specialized
bipeds. Although anatomical and physiological studies
on living humans documented sufficient conditions for
habitual bipedalism, it is difficult to discuss how capable those animals which exhibit a less specialized
condition are for bipedal behaviors. Specialized nonhuman bipeds, however, can be obtained under experimental conditions. Bipedal monkey attractions
have been developed widely in Asian countries since
ancient times. Japanese monkey performance, for
example, has a history of more than 1,000 years, and
is acknowledged as one of the most popular traditional entertainments in the country. Japanese macaques (Macaca fuscata) that engage in this traditional performance are trained to stand and walk
bipedally for about 1 hr daily (Hayama et al., 1992;
Iwamoto, 1985; Nakatsukasa and Hayama, 2003).
These macaques even develop a human-like lumbar
spinal curvature (Hayama et al., 1992; Preuschoft et
al., 1988). According to a computer simulations,
these trained monkeys are estimated to save one
third of the energy expenditure for bipedal walking
of ordinary experimental monkeys, owing to a more
erect posture of the trunk (Ishida, 1991). These macaques are thus excellent “experimental” bipeds,
and intriguing subjects for investigating the potential for bipedalism in nonhuman primates.
We report here on their locomotor energetics during
bipedal and quadrupedal walking. Whereas locomotor
energetics is an important aspect of foraging behavior
in animals (Steudel, 2000), experimental data have
rarely been accumulated since Taylor et al. (1982). In
particular, experimental studies detailing the energy
consumption for bipedal locomotion in nonhuman primates are very few. Taylor and Rowntree (1973) found
©
2004 WILEY-LISS, INC.
Grant sponsor: JSPS; Grant number: Grant-in-Aid 12440245.
*Correspondence to: Masato Nakatsukasa, Laboratory of Physical
Anthropology, Graduate School of Science, Kyoto University, Sakyo,
Kyoto 606-8502, Japan. E-mail: nakatsuk@anthro.zool.kyoto-u.ac.jp
Received 20 April 2002; accepted 22 May 2003.
DOI 10.1002/ajpa.10352
Published online 3 November 2003 in Wiley InterScience (www.
interscience.wiley.com).
LOCOMOTOR ENERGETICS IN JAPANESE MACAQUES
249
for bipedal performance since 2 years of age. Experiments were conducted from March 2001–June
2002.
Experimental procedures
Fig. 1. Body weight of subjects during experimental period.
No experiment was done on Subject 2 in November 2001.
that the energetic costs of bipedal and quadrupedal
running were the same in chimpanzees and capuchins.
Since then, no comparable study has been done. Thus,
this is the third study to compare locomotor energetics
in bipedal and quadrupedal locomotion in nonhuman
primates.
MATERIALS AND METHODS
Subjects
The subjects were two male Japanese macaques,
housed at the Suo Monkey Performance Association
(Kumamoto Prefecture, Japan). Among several
trained macaques, these two were best accustomed
to walking on a treadmill. This is an important
condition, because the subject is required to walk
continuously for 2– 6 min on a treadmill with stable
gait during the experiment (see below). There is no
particular strain or lineage of macaque for Japanese
monkey performance. In bipedal training done at
the Suo Monkey Performance Association, no restricting implements are used. The initial step of
training involves a bipedal stand exclusively, and
not a walk (Hayama et al., 1992). The trainer pays
particular attention to the degree to which the subject extends the hip, knee joints, and lumbar spine.
Each training session continues for 15–20 min and
is repeated several times a day. After a stable upright posture has been acquired, usually after a
week to a month, a long-distance walk can be accomplished with no difficulty. The Suo Monkey Performance Association is operated under municipal regulations regarding animal welfare and treatment.
Experiments were conducted with the collaboration of the Suo Monkey Performance Association,
following the guidelines for animal experimentation of Kyoto University.
Subject 1 was 9 years, 11 months in age at the
commencement of the experiments and had a body
weight of 11.6 –12.5 kg (Fig. 1). Subject 2 was 3
years, 11 months in age and had a body weight of
4.7– 6.2 kg (Fig. 1). Both subjects had been trained
Since we could not accustom the subjects to a
respirator gas mask, experiments were conducted
with subjects being placed in an airtight chamber
made of clear acrylic panels and an aluminum frame
(1.9 ⫻ 1.9 ⫻ 1.9 m), with the seams being coated
with silicone resin (Fig. 2). The chamber was fixed
on an acrylic floor sheet. The air-tightness of the
chamber was tested by releasing CO2 (carbon dioxide) into the chamber (ca. 2,000 ppm) and leaving it
overnight. A treadmill was carried into the chamber
during experiments. The subjects do not walk without the accompaniment of a trainer. Therefore, a
trainer remained within the chamber during the
course of the experiments while breathing through a
breathing tube extending from outside the chamber.
This condition necessitated a large chamber size and
was less conducive to the accurate determination of
gas concentrations in the chamber.
An infrared gas analyzer (Model CGT-7000, Shimadzu Corp.) was positioned in the chamber, and
CO2 concentrations were measured. Metabolic cost
is usually evaluated as a consumption of oxygen per
time and body mass (O2 ml/sec/kg). Thus, the evaluation of respiratory quotients (RQ ⫽ exhaled
CO2/O2 uptake) was necessary in order to determine
true metabolic cost. We were obliged to measure the
CO2 concentration because of the accuracy of the gas
analyzer. Reflecting the gas composition of the air
(O2 21 percent volume (vol%) vs. CO2 0.05 vol%), the
accuracy of standard O2 sensors is much lower (minimum scale, 10⫺2 vol%) compared to that of standard
CO2 sensors (10⫺4 vol%). This level of accuracy was
not proper for recording changes in O2 concentrations in our experimental chamber. However, we
tried to estimate RQ values in a later series of experiment (see below).
Ten electronic fans were set to enhance the diffusion of expired gas. Eight fans were set in corners of the chamber, and two were in front of and
behind the subject (Fig. 2). The air was sampled
from three positions on the wall and ceiling (arrows in Fig. 2). Sampling tubes were set to avoid
collecting expired breath of the subject directly.
Air mixing was checked preliminarily with a human being: a human came into the chamber and
stood near the position of the trainer (Fig. 2) for
more than 15 min. Soon after the chamber was
closed, the concentration of CO2 changed unstably. The inner air, however, then diffused evenly,
and a constant increase in CO2 concentration (resulting from breathing) was observed after 20 sec.
We conducted this test several times. A similar
pattern was also observed in experiments on macaques. Consequently, we began to record CO2
concentrations at least 30 sec after the chamber
was closed. The concentration of CO2 was recorded
250
M. NAKATSUKASA ET AL.
Fig. 2. Experimental chamber (left) and scene of experiment with Subject 1 (right). Air was sampled at three positions on wall and
ceiling (arrows), avoiding collection of expired breath directly.
Fig. 3. Change of CO2 concentration (open circles; ppm) and
O2 concentration (solid circles; vol%) against elapsed time (sec)
during an experimental session on Subject 1 (bipedal walk at 2.5
km/hr). CO2 and O2 concentrations (y) are linearly correlated
with elapsed time (x): y ⫽ 0.97x ⫹ 523.2 (r2 ⫽ 0.999) for CO2, and
y ⫽ ⫺1.4 ⫻ 10⫺4x ⫹ 21.07 (r2 ⫽ 0.998) for O2. Along regression
line of O2 concentration, RQ value between adjacent two plots is
indicated.
for at least 90 sec at intervals of 10 sec. Figures 3
and 4 show plots of CO2 concentration against
elapsed time. Experimental duration was variable
(90 –360 sec). Although there are some differences,
mean values are about 2 min in both bipedal and
quadrupedal sessions. Thus, the subjects walked
about 2.5 min in an average session (30 sec before
measuring, and about 2 min for measuring). Experiments were curtailed if the subject showed
signs of excessive tiring or irritation. When a subject ceased stable walking during an experimental
session, the data collected prior to cessation were
used or discarded completely. For this reason, the
duration of most experimental sessions was not
very long.
Each subject walked quadrupedally and bipedally
at a certain velocity (1.0/1.5– 4.5 km/hr) on the
treadmill within the chamber. Before the first experimental session, a test walk (warm-up) was conducted for more than 5 min, and consecutive sessions were separated by a resting interval of several
minutes. Walking velocity and mode of locomotion
(quadrupedal or bipedal) were changed at random.
Between sessions, the chamber was kept open. Air
refreshing was smoothly done, as enhanced by the
electronic fans.
The least-squares linear regression (LSR) was calculated between CO2 concentration and elapsed
time (Fig. 4). The regression was highly significant
in all sessions (r2 ⬎ 0.98). Taylor et al. (1982) noted
that when an animal begins to tire, its energetic cost
increases. Thus, a linear regression may not be fitted under conditions of extreme fatigue. However,
this was not the case in our experiments under
medium endurance.
The slope of the LSR was standardized using the
subject’s body weight, and was subsequently employed as a measure of energy consumption (␦CO2
ppm/sec/kg). The consumption of O2 can be calculated as (␦CO2 ppm/sec/kg ⫻ chamber capacity)/RQ.
The chamber capacity was 6,859 ⫻ 103 ml minus the
total volume of the experimental apparatus, trainer,
and subject. We ignored differences in body size of
trainers and of subjects when the LSR slope divided
by the subject body mass (␦CO2 ppm/sec/kg) was
used as a convenient measure of energy consumption, since these size differences were negligible relative to chamber size. The pressure within the
LOCOMOTOR ENERGETICS IN JAPANESE MACAQUES
251
Fig. 4. Increase of CO2 concentration (ppm) against elapsed time in (a) Subject 1 and (b) Subject 2. CO2 concentration was
measured each 10 sec from onset of session, and least-squares regression was calculated. Open circles and dotted lines represent
bipedal walk; solid circles and solid lines represent quadrupedal walk.
chamber throughout each experimental session was
assumed to be constant.
RQ
Our primary objective was a comparison of locomotor costs of bipedal and quadrupedal locomotion.
Thus, converting CO2 production to O2 consumption
was not essential for this study. The most important
point here was to prove that RQ did not fluctuate
significantly through all experimental sessions in
each subject. If this assumption were to hold, the
ratio of CO2 production rates (bipedalism to quadru-
pedalism) would be almost equivalent to the relative
metabolic cost of bipedalism in each subject. Some
evidence support this assumption.
The RQ is theoretically 1.0 under the aerobic combustion of glucose, and decreases if lipid or protein is
included in the respiratory substrate. Additionally,
part of the produced CO2 is stored in the muscle and
blood, resulting in a transient lowering of the RQ.
Figure 1 shows the body weights of subjects from
March 2001–June 2002. Although body weight is
basically stable in each subject, Subject 1 lost weight
in June 2001. However, the body weight loss did not
252
M. NAKATSUKASA ET AL.
TABLE 1. Respiratory quotients measured during bipedal
walking1
RQ relative to each decrease of
10⫺2 O2 vol%
Subject 1
2.5 km/hr
2.5 km/hr
3.5 km/hr
3.5 km/hr
3.5 km/hr
3.5 km/hr
Average
Subject 2
2.5 km/hr
2.5 km/hr
2.5 km/hr
3.5 km/hr
3.5 km/hr
3.5 km/hr
Average
4th2
Sessionaveraged
RQ
1st
2nd
3rd
0.73
0.68
0.98
0.70
0.61
0.61
0.72
0.79
0.71
0.66
0.74
0.70
0.52
0.70
0.63
0.60
0.82
0.80
0.69
0.71
0.71
0.82
0.75
0.66
0.57
0.703
0.63
0.53
0.73
0.58
0.59
0.70
0.63
0.57
0.76
0.79
0.57
0.69
0.74
0.69
0.66
0.51
0.63
0.54
0.61
0.80
0.63
0.62
0.60
0.72
0.56
0.63
0.75
0.653
0.83
0.55
1
RQs were calculated as increase of CO2 concentration while O2
concentration decreases by 10⫺2 vol%.
2
Duration of session: approximately 4 –5 min in Subject 1, and
4 – 6 min in Subject 2.
3
Mean of session-averaged RQs.
Fig. 5. Mass-specific CO2 production during 3.5-km/hr bipedal and quadrupedal walk in Subject 1 (␦CO2ppm/sec/kg ⫻ 10⫺2).
Solid diamonds, July 2001; open diamonds, June 2002. Although
Subject 1 lost weight in July 2001, no effect was observed.
affect mass-specific CO2 production by locomotor exercise (Fig. 5). Thus, it is unlikely that body fat or
muscles were particularly consumed as the respiratory substrate during this period. Since these subjects did not experience marked fat gain and loss, it
is possible to disregard body fat as a major respiratory substrate. These macaques are fed combinations of carbohydrate-rich food items (potato, beans,
maize, barely, and rice) with supplementary fruits
and vegetables. Although no menu was recorded
during the experiments, it is reasonable to predict
that animals fed such balanced diets would not have
extreme RQ values deviating from the normal range
(probably within 0.8 – 0.9).
During the latter series of experiments, we introduced an O2 sensor and measured both O2 and CO2
concentrations simultaneously in relatively long
sessions (Table 1). Calculated RQs were quite variable, not only between sessions but also within session. However, they showed correlation with neither
walking velocity nor duration. For two reasons, we
interpret the variability of RQ values as being
caused by the relatively low accuracy (or delay of
response) of the O2 sensor rather than the variability of true RQ itself; the variability of RQ is minor.
Firstly, CO2 production rates (B/Q ratios as well)
converged in a narrow range in each experimental
condition (Tables 2 and 3). If RQ is really as variable
as it appeared in Table 1 (e.g., 0.52– 0.98 in Subject
1 walking at a velocity of 3.5 km/hr), such constant
results are unexpected. Secondly, CO2 production
rates increase linearly as walking velocity increases
in each subject (Fig. 6). This regularity cannot be
expected if RQ values are highly variable. Figure 3
shows O2 consumption during a long session. O2
concentration seems to linearly decrease through
the session. However, calculated RQ values vary
from 0.6 – 0.83, even in this single session.
The average RQ was 0.7 in Subject 1 and 0.65 in
Subject 2 (Table 1). These values are extremely low,
particularly in Subject 2. It is impossible to give a
clear idea about the reasons for this. Possible causes
are a respiratory substrate involving more lipids
and CO2 storing in the body. However, the first
explanation is not sufficient for such extremely low
RQ values. Even if lipid was exclusively used as the
respiratory substrate, it should not be less than 0.7.
In addition, it is unlikely that lipid is preferentially
broken down as the respiratory substrate during
relatively short-term exercise. Also, we do not think
it is probable based on the diet of the subjects. The
second explanation is also unclear. If this is the case,
RQ values will rise with long exercise duration.
Such a tendency was not observed (Table 1). Since
these low values are not explainable, we did not use
these RQ values to obtain O2 consumption in our
subjects.
RESULTS
Table 2 and Figure 6a summarize the results of
experiments on Subject 1. Thirty-nine and 43 sessions were done for bipedal and quadrupedal walking, respectively. Subject 1 walked with velocities of
1.5– 4.5 km/hr. In both quadrupedal and bipedal
walking, %␦CO2 is correlated linearly with walking
velocities. The LSR formula between velocities and
mean %␦CO2 is: y ⫽ 1.961x ⫹ 2.156 (r2 ⫽ 0.957) in
bipedal walking, and y ⫽ 1.504x ⫹ 1.582 (r2 ⫽ 0.927)
253
LOCOMOTOR ENERGETICS IN JAPANESE MACAQUES
TABLE 2. CO2 concentration increase rates (ppm/sec/kg ⫻ 10⫺2) in bipedal and quadrupedal walking by subject 1
Walking velocity
Bipedalism
Mean
SD
n
Range
Mean duration of
session (sec)
Quadrupedalism
Mean
SD
n
Range
Mean duration of
session (sec)
B/Q ratio1
1
1.5 km/hr
2 km/hr
2.5 km/hr
3 km/hr
3.5 km/hr
4 km/hr
4.5 km/hr
5.37
0.09
5
5.26–5.46
120
6.48
0.54
6
5.72–6.94
103
6.55
0.56
5
5.99–7.37
126
7.60
0.70
9
6.91–8.82
113
9.06
0.13
5
8.91–9.16
154
9.62
0.71
6
8.85–10.72
111
11.59
0.59
3
10.91–11.97
116
4.05
0.54
5
3.59–4.93
120
4.87
0.62
6
3.91–5.69
127
5.10
0.36
4
4.60–5.45
120
5.67
0.55
10
4.97–6.92
110
6.93
0.76
5
5.76–7.85
148
6.98
0.73
10
5.88–7.72
100
9.05
0.56
3
8.41–9.46
127
1.33
1.33
1.29
1.34
1.31
1.38
1.28
Bipedal/quadrupedal ratio.
TABLE 3. CO2 concentration increase rates (ppm/sec/kg ⫻ 10⫺2) in bipedal and quadrupedal walking by subject 2
Walking velocity
Bipedalism
Mean
SD
n
Range
Mean duration of
session (sec)
Quadrupedalism
Mean
SD
n
Range
Mean duration of
session (sec)
B/Q ratio1
1
1 km/hr
1.5 km/hr
2 km/hr
2.5 km/hr
3 km/hr
3.5 km/hr
4 km/hr
4.5 km/hr
7.15
0.89
4
5.84–7.78
98
6.08
0.22
4
5.84–6.37
123
8.65
0.77
4
7.90–9.72
100
7.94
0.42
6
7.31–8.37
148
9.66
0.72
9
8.51–10.59
123
10.61
0.80
6
9.66–11.95
132
11.56
0.59
5
10.89–12.36
102
12.04
1.31
2
11.11–12.96
120
5.98
0.11
3
5.85–6.08
120
6.28
0.50
5
5.73–6.87
102
6.45
0.72
4
6.07–7.59
140
7.75
0.53
6
6.77–8.22
100
8.50
1.08
4
7.80–10.10
147
9.61
0.25
3
9.43–9.78
110
1.02
1.38
1.23
1.25
1.25
1.20
10.01
1.24
2
9.19–10.88
140
1.20
Bipedal/quadrupedal ratio.
in quadrupedal walking. Slopes are not significantly
different between these LSR trajectories (P ⫽
0.852). The bipedal/quadrupedal ratio of %␦CO2 is
rather constant, ranging from 1.28 –1.38, with an
average of 1.32.
Table 3 and Figure 6b summarize the results of
experiments on Subject 2. Forty and 27 sessions
were conducted for bipedal and quadrupedal walking, respectively. Subject 2 walked with velocities of
1.0 – 4.5 km/hr. No data could be gathered on quadrupedal walking at a velocity of 1.0 km/hr. Although %␦CO2 is generally correlated with velocities
for both quadrupedal and bipedal walking, the variation is large for bipedal walking at low velocities.
This result probably reflects that these velocities
(ⱕ1.5 km/hr) were too low for this subject to accomplish stable walking (Hirasaki, unpublished data).
At a velocity of 2.5 km/hr, %␦CO2 drops markedly in
both bipedal and quadrupedal walking. Gaits at
walking velocities faster than 2.0 km/hr were fairly
stable (unpublished data); the reason for this is unclear. At higher velocities, %␦CO2 increases linearly,
and bipedal/quadrupedal ratios of %␦CO2 are fairly
constant, at around 1.2. LSR lines are calculated as:
y ⫽ 1.65x ⫹ 4.68 (r2 ⫽ 0.901) for bipedal walking,
and y ⫽ 1.486x ⫹ 3.34 (r2 ⫽ 0.960) for quadrupedal
walking. There is no significant difference of slopes
between these LSR trajectories (P ⫽ 0.1079).
Although the trials were much less abundant, we
conducted a further experiment. Subject 1 walked
quadrupedally at a certain velocity for about 2 min,
and then switched locomotor mode to bipedalism,
and continued to walk at the same velocity. Figure 7
indicates a change of CO2 concentration through the
session. The walking velocities were 1.5, 3.0, and 4.0
km/hr. After the locomotor mode was switched to
bipedalism, CO2 production significantly increased
in all trials (shown in the slope of the LSR line). The
B/Q ratio in each velocity is 1.15 (1.5 km/hr), 1.19
(3.0 km), and 1.17 (4.0 km). Although all of these
values are rather lower than the B/Q ratio calculated from averaged values in multiple sessions (Table 2), this result clearly proves that a bipedal walk
costs significantly more than a quadrupedal walk.
DISCUSSION
The experimental conditions in this study were
different from those in previous studies. For example, subjects in Taylor et al. (1982) were intended to
run with greater endurance (15–30 min) than would
normally be required in nature. Running velocities
in their experiments reached as high as 11 km/hr.
254
M. NAKATSUKASA ET AL.
Fig. 7. CO2 concentration (ppm) increase in quadrupedal and
bipedal walking by Subject 1 (walking velocities: 1.5, 3.0, and 4.0
km/hr). Locomotor mode was switched from quadrupedalism to
bipedalism at middle of session (indicated by arrow). After
switching to bipedalism, CO2 production significantly increases
in all trials (shown in slope of LSR line). LSR slopes and 95%
confident limits are shown.
Fig. 6. Standardized CO2 concentration increase rates (ppm/
sec/kg ⫻ 10⫺2) in bipedal and quadrupedal walking with different
velocities (km/hr) in Subject 1 (a) and Subject 2 (b). Mean ⫾ 1
standard deviation. Diagonal lines are LSR trajectories: y ⫽
1.961x ⫹ 2.156 (r2 ⫽ 0.957) in bipedal walking, and y ⫽ 1.504x ⫹
1.582 (r2 ⫽ 0.927) in quadrupedal walking in Subject 1; y ⫽
1.65x ⫹ 4.68 (r2 ⫽ 0.901) for bipedal walking and y ⫽ 1.486x ⫹
3.34 (r2 ⫽ 0.960) for quadrupedal walking in Subject 2.
Their experimental conditions reflected the different
purpose of their study. They aimed to compare locomotor energetic physiology in diverse warm-blooded
animals. On the other hand, we focused on a more
restricted comparison: the difference in energetic
cost for bipedalism and quadrupedalism in the same
individual. Because our experiments were carried
out with relatively short durations, critics may question the rigorousness of our estimates of energetic
costs. It is generally thought that at least 4 min is
necessary for an animal to reach a steady state from
onset of exercise. If we measured presteady-state
energetic cost, observed values would be higher than
those at a steady state (Taylor et al., 1982). In several sessions with a relatively long duration (e.g.,
Fig. 3), CO2 production rates, however, appear almost constant through the session (ⱖ5 min), and
there is no tendency for them to decrease in the later
part of a session. This probably indicates that the
exercise in our subjects was mostly supplied by the
aerobic system, and that contributions from the anaerobic system, if any, were negligible. The relatively short experimental duration suggests that
subjects did not yet reach a steady state. However,
we have measured energetic costs for bipedalism
and quadrupedalism under the same conditions (including costs for start-up). Thus, the comparisons
should be relevant in evaluating the relative energetic costs of bipedal walkng in each subject.
Since Taylor et al. (1982), comparative locomotor
energetics in nonhuman primates have rarely been
investigated. In particular, studies detailing meta-
LOCOMOTOR ENERGETICS IN JAPANESE MACAQUES
bolic costs associated with nonhuman primate bipedal walking are limited. Unfortunately, the methodological problems in this study, and particularly the
uncertainty of true RQ, pose difficulties in comparisons with previous studies. However, if we credit
the assumption that fluctuation of RQ is negligible,
some comparison is possible. It is known that massspecific O2 consumption is linearly correlated with
walking/running velocities (Taylor et al., 1982). This
is also the case in our study. Taylor et al. (1982)
published energetic costs of quadrupedal walking in
an 8.5-kg hamadryas baboon and a 5.1-kg stumpedtailed macaque. If a seemingly appropriate RQ is
given (e.g., 0.8 – 0.9), the observed mass-specific CO2
production in our subjects yields similar values of
mass-specific O2 consumption as in these equivalent-sized monkeys.1 This may give credibility to our
estimates of locomotor energetics.
Despite several methodological problems in our
experiments, Figure 7 indicates higher energetic
costs in bipedal walking, without a doubt. The only
remaining uncertainty is the degree of difference.
The B/Q ratios in the single-session experiments are
lower than those calculated from averaged data in
multiple sessions (Tables 2 and 3). Since the number
of trials is only three, it is not clear if this difference
is biologically meaningful or produced by chance,
and (if the former is the case) what causes this
difference. More trials are needed, and similar experiments with the reverse sequence (bipedalism to
quadrupedalism) are also necessary.
Taylor and Rowntree (1973) noted that the energetic costs for bipedal and quadrupedal walking
were the same for chimpanzees and capuchins at
velocities of 1.5–5 km/hr. In our results, however,
the energetic cost for bipedalism was higher by
20 –30% than that of quadrupedalism in both subjects, regardless of walking velocity (1.5– 4.5 km/
hr). Despite the chance that we included data at
presteady state, this does not explain the contradicting results, because the experimental conditions (e.g., walking duration) were the same in
bipedal and quadrupedal walking. One exception
was Subject 2, at a velocity of 1.5 km/hr (Fig. 4b),
which is too slow for comfortable voluntary walking in Japanese macaques.
Why have these two studies produced different
results? Since the energetic cost for quadrupedalism
in chimpanzees is very high compared to the general
mammalian standard (⫹36%; Taylor et al., 1982),
the “relatively low” energetic cost of bipedalism
might not be surprising for chimpanzees. However,
the same explanation is not possible for capuchins,
which are more efficient quadrupeds (only 10% extra
1
Mass-specific CO2 production rates can be converted to massspecific O2 consumption (mlO2/sec/kg) as follows: (CO2 values given in
Tables 2 and 3) ⫻ 0.0676/RQ. For example, mass-specific O2 consumption in Subject 2 walking at a velocity of 3.5 km/hr (⫽ 0.97 m/sec) is
0.68 (when RQ is 0.85). This value almost coincides with data of a
5.1-kg stumped-tailed macaque in Figure 1C in Taylor et al. (1982).
255
cost; Taylor et al., 1982). There are a few possible
explanations. One is that the relatively cheap cost of
bipedalism in capuchins can be accounted for by
their smaller body size (on average, 3.34 kg), as the
excess energetic cost in bipedalism was lower in the
younger Subject 2 than in Subject 1 (Tables 2 and 3).
However, Subject 2 was 4.2 kg at the beginning of
the experiment, and the size difference for the capuchins was less than 1 kg. Thus, this explanation is
weak. Another explanation might be that Japanese
macaques are particularly inefficient bipeds. Biomechanical analysis by Yamazaki (1985) revealed that
ordinary experimental Japanese macaques have relatively low potential abilities for bipedal walking
when compared with gibbons, chimpanzees, and spider monkeys. Undoubtedly, these trained macaques
are extremely adept walkers compared with most
other nonhuman primates. However, genetically determined anatomical features might entail more extra energetic costs than in capuchins. This seems
likely, because high muscular activities would be
required in macaques to maintain hindlimb joints in
flexed positions and to control excursions of the center of gravity (Hirasaki et al., 2002), even if the
forelimbs are almost free from body support and
driving. In capuchins, the tails might have partly
contributed to balancing the trunk. It would be necessary to examine the kinematics and/or kinetics of
capuchin walking to discuss this possibility.
Whatever the reason may be, it must be remembered that comparative studies of this kind are extremely few. Caution should thus be exercised in
generalizing from the arguments of Taylor and
Rowntree (1973) to other primates.
However, is the energetic cost of bipedal walk
really great for these trained macaques? When Ateles travel by suspensory locomotion, energy consumption is 30 – 40% greater than in quadrupedalism (at 2 km/hr; Parsons and Taylor, 1977). This
excess ratio is even greater than the B/Q ratio in
trained macaques. Bipedal walking cost at 2 km/hr
was as much as quadrupedal walking cost at 3.0
km/hr in Subject 1, and bipedal walking at 2.5 km/hr
cost as much as quadrupedal walking at 3.6 km/hr
(Fig. 3). In Subject 2, the bipedal walking cost at 2
km/hr was equivalent to the quadrupedal walking
cost at 3.2 km/hr, and bipedal walking at 2.5 km/hr
cost as much as quadrupedal walking at 3.8 km/hr.
Extra locomotor costs at this amount might be compensated by benefits obtained through bipedalism.
We observed two skeletons of trained monkeys
which died of acute disease (13 and 9 years in age).
Apart from a thickened cortex and somewhat enlarged articular surfaces (Nakatsukasa et al., 1995;
Nakatsukasa and Hayama, 2003), these skeletons
did not exhibit severe degenerative articular
changes or vertebral body deformations. This observation suggests that stresses to the skeletal system
introduced by bipedal behaviors with medium en-
256
M. NAKATSUKASA ET AL.
durance were at a tolerable level throughout their
lives.2
The locomotor kinematics of Subjects 1 and 2 are
currently being analyzed and will be published elsewhere. Hirasaki et al. (2002) preliminarily revealed
several kinematic features of bipedal walking which
may improve locomotor efficiency in these trained
macaques. These trained monkeys exhibit less frequent but longer strides than in untrained macaques. The hip-joint trajectory follows an upward
convex curve during the support phase, resembling
the inverted pendulum movement in human bipedalism. Angular movements of the head and trunk
are reduced compared to those of ordinary macaques. These characteristics are common among
trained macaques, despite individual variations.
Thus, it is intriguing to evaluate how much the
bipedal energetic cost is reduced in these macaques
relative to the cost in ordinary macaques. Unfortunately, we have not yet succeeded in measuring the
locomotor energetic cost of ordinary macaques in the
same experimental setup, because those animals
could not walk with constant gaits for as long as 2
min. Heart pulse rates, however, are a good measure
of energy expenditure (Rose and Gamble, 1994), and
can be more easily monitored. We are attempting to
compare locomotor energetic by doing so. We have
observed that bipedal gait becomes more stable
through training in trained macaques. Longitudinal
studies as well as studies of individual variation of
locomotor energetics and kinematics/kinetics will
reveal how much energy is saved in trained macaques in relation to different gait and postural patterns, and may shed some light on the adaptive
processes of bipedalism in the earliest hominids.
ACKNOWLEDGMENTS
We are very grateful to the trainers and macaques
of the Suo Monkey Performance Association for their
2
We observed a severe pathological deformation of the hip joint in a
wild subadult Japanese macaque which congenitally lacked both forearms and had necessarily adopted bipedalism for traveling (Nakatsukasa, personal observations). This case suggests that a complete
transition to bipedalism introduces too much stress to the skeletal
system of the Japanese macaque. The kinematics of bipedal walking
in this macaque were more ordinarily monkey-like than in a trained
macaques (Ogihara, unpublished findings).
enormous patience in carrying out the repetitive
experiments required of this investigation. We
thank K. Steudel-Numbers and other reviewers for
thoughtful comments on our manuscript, and M.D.
Rose for English-language editing of the manuscript. Many thanks go to H. Sato, J. Domoto, E.
Ishizaki, A. Hidaka, and Shimadzu Medical Systems
Corp. for kind advice and support in setting up the
experimental system.
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