the foot force between the forelimb and the hindlimb did not largely change with a ... arboreal primates, for which the hindlimb was clearly dominant in their ...
PRIMATES, 33(4): 465-476, October 1992
465
Hindlimb Dominance During Primate High-speed Locomotion TASUKU KIMURA
Kyoto University
ABSTRACT. Quadrupedal locomotion was mechanically studied for four species of primates, the chimpanzee, the rhesus macaque, the tufted capuchin, and the ring-tailed lemur, from low to high speeds of about two to ten times the anterior trunk length per second. A wide variety of locomotor patterns was observed during the high-speed locomotion of these primates. Positive correlations were observed between the peak magnitude of foot force components and speed. The differentiation of the foot force between the forelimb and the hindlimb did not largely change with a change of speed for each species. The vertical component and the accelerating component for the rhesus macaque were relatively large in the forelimb from low- to high-speed locomotion. The rhesus macaque, which habitually locomotes on the ground, differed in the quadrupedal locomotion from the other relatively arboreal primates, for which the hindlimb was clearly dominant in their dynamic force-producing distribution between the forelimbs and the hindlimbs. The previously reported locomotor difference, which was indicated among primates from the foot force pattern between the forelimb and the hindlimb during walking, also applied to high-speed locomotion. Key Words: Speed; Gallop; Running; Foot force; Arboreal. INTRODUCTION The quadrupedal walking of n o n h u m a n primates shows many different characteristics compared with that of c o m m o n terrestrial m a m m a l s (KIMURA et al., 1979; KIMURA, 1985). Within the order of primates, two groups are observed on the quadrupedal walking especially from the view point of the force plate studies. The first group consists of the chimpanzee, the orangutan, and the spider monkey, and the second group of the Japanese macaque and the hamadryas baboon. The latter group, which habitually move by quadrupedal locomotion on the ground, show a relatively large magnitude of foot force in the forelimbs. This characteristic is relatively closer to that of the c o m m o n terrestrial m a m mals, the foot force of which is usually larger in the forelimbs than in the hindlimbs for the vertical and accelerating components. Habitual "locomotor repertoires of the former group include quadrupedalism and climbing in the trees. Their capacities for body weight bearing and acceleration are clearly larger in the hindlimbs than in the forelimbs. This characteristic may be related to a preadaptation for h u m a n bipedalism. This paper is concerned with the quadrupedal primates moving at different speeds on a level surface, especially with the characteristics measured by means of force plate analysis. The fore- or hindlimb dominance was investigated in each species of primates studied. The differences of high-speed locomotion a m o n g the primates and the influence of speed on foot force are discussed. SUBJECTS A N D M E T H O D S Four species, one species each from the apes, Old World monkeys, New World monkeys,
466
T. KIMURA
Table 1. Subjects. Species
Number
Age
Sex
Body mass (kg)
Trunk length* (mm)
Chimpanzee Rhesus macaque Tufted capuchin Ring-tailed lemur
3 3 1 1
2y0m @-Adult ca. 10y lyl0m
IM 4- 2F 1M + 2F M F
9.0 - 10.2 5.2 - 7.3 3.3 3.1
258 - 274 317 - 378 248 218
*See the page 467.
and prosimians, were studied. They were three chimpanzees (Pan troglodytes), three rhesus macaques (Macaca rnulatta), one tufted capuchin (Cebus apella), and one ring-tailed lemur (Lemur catta) (Table 1). Due to the restriction of the size of the laboratory, it was necessary to use small animals. All chimpanzees were 2-year-old infants. The ring-tailed lemur was also a young individual. The animals locomoted on a level wooden platform in a 5m long laboratory. The platform was about 4m in length and about 0.5m wide. A force plate (Sogo Keiso TRo61200) was placed in the middle of the platform, which was divided into six parts. Contact signals for the fore and hind feet were obtained by switches attached to each part of the platform. When a foot of the animal was placed on a portion of the platform, an electrical signal was recorded on an oscillograph along with the force plate data. The animals moved about freely on the platform without any attachments on the body. The chimpanzees were trained to go back and forth on the platform, though their pattern and the speed of locomotion were not particularly restricted. A cage approximately 65cm high covered the platform during the trials for the other three species. They moved freely within the cage. The foot force was decomposed into three components: vertical, sagittal, and transverse. Any oscillations higher than 50Hz were removed. The force was divided by the body weight (BW in this paper) to produce a ratio which canceled the differences in the body mass among the subjects. The sagittal component was further subdivided into the braking component during the braking duration and the accelerating component during the accelerating duration. The mean components during the cycle of locomotion were calculated from the impulses of the components divided by the cycle duration as follows (Fig. 1):
VM
--
, BM
-
, AM
Dc
--
Dc
,
Dc
TM
--
,
Dc
where Vis the vertical component, B is the braking component, A is the accelerating component, T is the transverse component, M indicates the mean component, Dc is the cycle duration, Ds is the stance phase duration, and DB is the braking duration. In an ideal uniform motion, the sum of the mean components of the four limbs equals the body weight in the downward component, and is zero in the sagittal and transverse components as follows: H
H
H
H
H
Z VM = 1, ~ S M = E B M + Z A M = O, Z T M = O,
Primate High-speed Locomotion
467
BW 13.25 T out
tn 13.25 A 13.'25T11 br~k~
$13
~/p
13.25 1.13
/ij I
~0 W~
V13.5
.~/.l,~r~'rJ.ris, r 4 . 1 " -r.v.v.v.vrl ~"
13 -~Dc
sg'5
Fig. 1. Mean components. The mean component is calculated from the impulse of a component during the stance phase duration (STD) divided by the cycle duration (CD). The leading forelimb of a galloping 2-year-old chimpanzee is shown in the figure as an example. The hatched area shows the impulse of the component. The size of the hatched area (impulse) in the vertical component is the same as that of the dotted area (mean component multiplied by the cycle duration). The broken line shows the components of the trailing hindlimb. V: Vertical component; S: sagittal component; T: transverse component; BW: body weight; BD: braking duration.
where S is the sagittal component and n is the number of limbs, which is four in this case. The side view o f motion for the subjects in the sagittal plane was recorded using a 16ram cinecamera or a video tape recorder situated at a distance of about 7m from the platform. The distance o f progression was measured by motion analysis. This distance was then divided by anterior trunk length (length from suprasternale to symphysion: TL in this paper, see Table 1) in order to produce a ratio which eliminated the differences in the body size among the subjects.
RESULTS Many varieties of locomotor pattern were observed during the experiments. Walking consisted of symmetrical gaits with a forward cross type footfall order (IWAMOTO& TOMITA, 1966). High-speed locomotion observed in the experiment was mainly an asymmetrical gait during which the posture of locomotion was that of the gallop, that is, two forelimbs and two hindlimbs moving partially in pairs with the back of the body being flexed and extended alternately. This locomotion is called " r u n " in this paper. Cases of galloping during which all four limbs were simultaneously in the air were observed. However, not all trials of the " r u n " included a stage of suspension. Some trials of canter were observed. In the canter, each pair o f lateral limbs are alternately lifted and placed on the ground around the same time. Many trials of high-speed trot were observed in the rhesus macaques. During the trot, the diagonal pair of limbs are used more or less in synchrony, instead of lateral pairs as in the canter. In the cases o f high-speed canter and trot, the stance phase duration of the forelimb or hindlimb was less than half of the cycle duration. These types of high-
468
T. wALK
RUN
Chimpanzee
R,Macaque
L
H
R.T.Lemur
J
I
L H F
,-,,--I
I I
I
I I
1
b
I
I
I
I
J
i
F
I
I
I
H
I
I I
I
F
F R H H L F F R H
0.5
L
1
L H
T.Capuchin
0
I
F "~
R
0.5
1
F R H
KlmurA
I,
I I
I
I
I I
1
I I I
j
I
I
I
I
j
I 1
I
I
I
N I
I
b
I I I Fig. 2. Examples of footfall sequences. The trial of "run" in the chimpanzee is a rotatory gallop. "Run" in other species is the transverse gallop. The footfall order during walk in all species is the forward cross type. L: Left; R: right; H: hindlimb; F: forelimb.
speed l o c o m o t i o n were included as "run" in the results. During high-speed locomotion, no instances of leap or ricochet were observed in the present experiments. Some cases o f crutch walking by the chimpanzee were excluded from the results. Examples o f tripedal and bipedal walking by the chimpanzee and the lemur were also excluded. Examples of footfall sequence are shown in Figure 2. The maximum speeds observed were 9.56 TL/s in the chimpanzee, 11.64 TL/s in the macaque, 13.88 TL/s in the capuchin, and 7.82 TL/s in the lemur. The minimum speeds observed were 1.96, 1.65, 2.12, and 1.78 TL/s in the chimpanzee, the macaque, the capuchin, and the lemur, respectively. The average speed o f the "run" was higher than that of walking in all species (Fig. 3). A high-speed was usually obtained both by a short cycle duration and by a long stride length. There was a significant positive correlation between stride length and speed in all species (Fig. 4). The cadence, the number of cycles per time, was positively correlated with speed in all species.
Cycle
Duration
Stride
Length
Speed
N 0,5
sec
2.5
TL
5 f
I
Chimpanzee ~
47 .Z.X.X.Z.X,_'.X.~:~;~;~:~X~
3647
R.Macaque ~ 6~ ~
J
,
R 24
16 ~ . Z " . " . ' F . X . F 20
W 40
r.T.Lemor
~ ~ ~
~ I
I0
3647 .V.....V...v...V....:~:lI - ,
50
T.Capuchin
TL/sec
~
12 v.'.v.v.v.'.'.v,'.v.v.v.'X'X'X.Z,:'~--
9
~ I
Fig. 3. Cycle duration, relative stride length, and relative velocity. The mean and one standard deviation are shown. The stride length and the speed are divided by the anterior trunk length (TL). R: Run , W: walk; N: number of trials.
Primate High-speed Locomotion
469
T. CAPUCHIN i5
,/
LL~ + ++
t /
, 5
TL
STRIBE
fi
I/5
S
CfiDENCE
LENGTH
Fig. 4. Correlations of relative stride length and cadence with relative speed in the tufted capuchin. Cadence is the number of cycles in a second. Linear regressions are significant. Cross: Walking; circle: "run". The relative stance phase duration, that is, the stance phase duration divided by the cycle duration, became shorter when the speed increased. The correlation coefficients of the relative stance phase duration and speed were significant in all limbs except the forelimb o f the chimpanzee. The relative stance phase duration o f the "run" was shorter than that o f the walk (Fig. 5). The relative stance phase duration of the hindlimbs was significantly longer than that o f the forelimbs in the "run" of the tufted capuchin and the ring-tailed lemur. The vertical mean component o f the "run" was significantly larger in the hindlimb than in the forelimb in the case o f the tufted capuchin (Fig. 6). In contrast, it was significantly N 0
F
Chimpanzee R H W
R.Macaque
36 3l 32 30
~
H
R F
24
~
F H F
H 2O
Cycle
].-I H
8 7 57 46
R W
T.Capuchin
0.5
Z-Z,:.:.Z,2.:.:.:,X-Z,FF--~
W ~ s9
4O
R
R.T.Lemur
w
H 9 F ~9 H
I.----t
19
I
Fig. 5. Relative stance phase duration. Stance phase duration divided by the cycle duration. Mean and one standard deviation are given. R: "Run"; W: walk; F: forelimb; H: hindlimb. Significant differences between the forelimbs and the hindlimbs. *p < 0.05; **p < 0.01.
470
Z KIMURA Mean Vertical 0.25
Chimpanzee
R F
Component Transverse in
down
BW 0 . 5
20 19
H
out
-0.05
BW
0
8.05
18 i
WH
3
~
R.Macaque R F
T.Oapuchin
II
H F 1~ I;'] H
P-~p__~
:-:.:5.:5.:.:.:.:.:.:.5:.:.5:.:-:-:;.:-:-}'---'1* * *
3
10 3 3
:':':':':':':':':':':':':':'3:':':':-:.:.:.:':.:]
R.T.kemur
I
1
I
""~-~
] 3
+:'X':':
1
J
I
I
Fig. 6. Mean components in vertical and transverse directions. BW: Body weight. *p
