Kinematic adjustments to arboreal locomotion in Japanese macaques (Macaca fuscata).

Although biomechanical adaptations to arboreal locomotion have been well investigated in primates and other mammals in laboratory settings, the results are not consistent, and more species need to be studied to build a comprehensive picture of this. Here, we used three-dimensional videography to quantify kinematic parameters thought to be associated with locomotor stability while two Japanese macaques walked on terrestrial and simulated arboreal substrates (a horizontal pole, which was narrow relative to the animal's body width). The parameters investigated included temporal-spatial gait variables, those associated with compliant walking, the height of the shoulder and hip, and hand and foot clearance during the swing phase. We found that there were many individual differences in kinematic adjustments made by the monkeys during arboreal locomotion. More importantly, the results were consistent between the monkeys for three parameters: maximum hand clearance, maximum hip height, and maximum foot clearance. The monkeys showed lower maximum hand and foot clearances during arboreal locomotion than during terrestrial locomotion, indicating that the hands and feet were kept close to the substrate surface during the swing phase. They also showed lower maximum hip heights during arboreal locomotion, suggesting that their whole-body centers of mass were lowered. These consistent kinematic adjustments can be interpreted as strategies for enhancing stability and reducing the risk of falling from a height. Overall, these results show that Japanese macaques make significant biomechanical adaptations to arboreal locomotion that are not fully consistent with existing data for other animals.

Muscle Spindle Density of Lateral Rotators of the Thigh in Japanese Macaques and a Gibbon.

We examined the six small lateral rotators of the hip joint, which is one of the most flexible joints and allows kinematically complex motions of the hindlimb, to elucidate the functional differentiation among these muscles and to test the hypothesis that species-specific characteristics in hindlimb use during locomotion are reflected in the muscle spindle density and in other parameters of the deep small hip joint rotators. For these purposes, we estimated the number of muscle spindles of the superior gemellus muscle (SG), inferior gemellus muscle, quadratus femoris muscle, obturator internus muscle (OI), obturator externus muscle, and piriformis muscle in three Japanese macaques and a gibbon, using 30-µm-thick serial sections throughout each muscle length after azan staining. The numbers of muscle spindles per 10,000 muscle fibers were determined to compare inter-muscle variation. The spindle density was highest in the SG and lowest in the OI in the Japanese macaques, suggesting that the SG, which is attached to the tendon of the OI, functions as a kinesiological monitor of the OI. On the other hand, SG the was missing in the gibbon, and the OI in the gibbon contained more spindles than that in the Japanese macaques. This suggests that the SG and the OI fused into one muscle in the gibbon. We postulate that the relative importance of the deep small hip rotator muscles differs between the Japanese macaques and gibbon and that the gibbon's muscles are less differentiated in terms of the spindle density, probably because this brachiating species uses its hindlimbs less frequently.

Intra-individual variation in hand postures during terrestrial locomotion in Japanese macaques (Macaca fuscata).

The primate hand adopts a variety of postures during locomotion. Habitually terrestrial cercopithecine primates are known to use a palmigrade posture at faster speeds to possibly mitigate stresses on the hand skeleton; however, it is unclear whether arboreal or semi-terrestrial species use a similar strategy for adjusting hand posture. Here, we explored intra-individual variation in hand contact patterns during terrestrial locomotion in the Japanese macaque (Macaca fuscata), a semi-terrestrial cercopithecine primate. Two monkeys were required to walk on the ground at their own preferred speeds or were encouraged to move faster for food rewards. The contact area under the hand and ground reaction forces (GRFs) were measured simultaneously using a tactile pressure sensor, and then hand pressures were calculated offline. We found that hand contact patterns could vary within individuals. The monkeys used predominantly a palmigrade posture within the range of speeds covered in this study (0.72-2.56 m s-1). There were two subtypes of palmigrade posture. In one subtype, the hypothenar pad did not contact the substrate, whereas the entire hand contacted the substrate in the other. The palm of the palmigrade hand with total-hand contact experienced similar or lower peak pressure and pressure-time integral than those of the palmigrade hand without hypothenar pad contact even though it experienced higher peak GRFs. The moderate peak pressure experienced by the palmigrade hand with total-hand contact was due to increased contact area under the palm. The total contact area of the fingers and peak GRF to the fingers were relatively unchanged with different patterns of hand contact. These findings provide evidence that when walking on the ground, semi-terrestrial Japanese macaques use a palmigrade posture with total-hand contact to attenuate stresses on hand bones, as do habitually terrestrial species.

The estimated mechanical advantage of the prosimian ankle joint musculature, and implications for locomotor adaptation.

In this study we compared the power arm lengths and mechanical advantages attributed to 12 lower leg muscles across three prosimian species. The origins and insertions of the lower leg muscles in Garnett's galago, the ring-tailed lemur, and the slow loris were quantified and correlated with positional behaviour. The ankle joint of the galago has a speed-oriented mechanical system, in contrast to that of the slow loris, which exhibits more power-oriented mechanics. The lemur ankle joint exhibited intermediate power arm lengths and an intermediate mechanical advantage relative to the other primates. This result suggests that the mechanical differences in the ankle between the galago and the lemur, taxa that exhibit similar locomotory repertoires, reflect a difference in the kinematics and kinetics of leaping (i.e. generalised vs. specialised leapers). In contrast to leaping primates, lorises have developed a more power-oriented mechanical system as a foot adaptation for positional behaviours such as bridging or cantilevering in their arboreal habitat.

Brief communication: Three-dimensional motion analysis of hindlimb during brachiation in a white-handed gibbon (Hylobates lar).

In brachiating gibbons, it is thought that there is little movement in the hindlimb joints and that lateral body movement is quite limited. These hypotheses are based on naked-eye observations, and no quantitative motion analyses of the hindlimbs have been reported. This study quantitatively describes the three-dimensional movements of the lower trunk and distal thigh during continuous-contact brachiation in a white-handed gibbon (Hylobates lar) to evaluate the roles of the trunk and hindlimb. The results revealed that the lower trunk moved both laterally and vertically. The lateral movement of the lower trunk resulted from the lateral inclination of the trunk by gravity. The vertical movement of the trunk was converted into forward velocity, indicating an exchange between potential and kinetic energy. We also observed flexion and extension of the hip, although the excursion was within a small range. In addition, the lateral movement of the hindlimb in thedirection opposite to that of trunk movement helped to reduce the lateral sway of the body. These results suggest that during continuous-contact brachiation a gibbon uses hip flexion and extension motions to increase the kinetic energy in the swing. In addition, fine motions of the hip may restrict the lateral sway of the center of body mass.

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

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.

Gaits of Japanese macaques (Macaca fuscata) on a horizontal ladder and arboreal stability.

Most primates use diagonal sequence (DS), diagonal couplets (DC) gaits when they walk or run quadrupedally, and it has been suggested that DSDC gaits contribute to stability in their natural arboreal habitats compared to other symmetrical gaits. However, this postulate is based solely on studies of primate gaits using continuous terrestrial and arboreal substrates. A particular species may select suitable gaits according to the substrate properties. Here, we analyzed the gaits of Japanese macaques moving on a horizontal ladder with rung intervals ranging from 0.40 to 0.80 m to elucidate the relative advantages of each observed form of gait. The rung arrangement forced our macaques to choose either diagonal coupling or DS gaits. One macaque consistently used diagonal coupling (i.e., DSDC and LSDC gaits) across narrow and intermediate rung intervals, whereas the other macaque used DS gaits (i.e., DSDC and DSLC gaits). At wider rung intervals, both macaques shifted to a two-one sequence (TOS), which is characterized by two nearly simultaneous touchdowns of both forelimbs and one touchdown of each hind limb in a stride. The transition to the TOS sequence increased the duration of support on multiple limbs, but always included periods of a whole-body aerial phase. These results suggest that Japanese macaques prefer DSDC gaits, because the diagonal coupling and DS contribute separately to stability on complex supports compared to the lateral coupling and lateral sequence. We also postulate that stability triggers the transition from symmetrical gaits to the TOS sequence.

Ground-reaction-force profiles of bipedal walking in bipedally trained Japanese monkeys.

Ground-reaction-force (GRF) profiles of bipedal locomotion in bipedally trained Japanese macaques (performing monkeys) were analyzed in order to clarify the dynamic characteristics of their locomotion. Five trained and two ordinary monkeys participated in the experiment. They walked on a wooden walkway at a self-selected speed, and three components of the GRF vector were measured using a force platform. Our measurements reveal that trained monkeys exhibited vertical-GRF profiles that were single-peaked, similar to those of ordinary monkeys; they did not generate the double-peaked force curve that is seen in humans, despite their extensive training. However, in the trained monkeys, the peak appeared relatively earlier in the stance phase, and overall shape was more triangular than that of the more parabolic profile generated by ordinary monkeys. Comparisons of vertical fluctuation of the center of body mass calculated from the measured profiles suggest that this was larger in the trained monkeys, indicating that storage and release of potential energy actually took place in their bipedal walking. This energetic advantage seems limited, however, because efficient exchange of potential and kinetic energy during walking were not completely out of phase as in human walking. We suggest that anatomically restricted range of hip-joint motion impedes the inherently quadrupedal monkeys from generating humanlike bipedal locomotion, and that morphological rearrangement of the hip joint was an essential precondition for protohominids to acquire humanlike bipedalism.

Density of muscle spindles in prosimian shoulder muscles reflects locomotor adaptation.

We examined the correlation between the density of muscle spindles in shoulder muscles and the locomotor mode in three species of prosimian primates: the slow loris (Nycticebus coucang), Garnett's galago (Otolemur garnettii), and the ring-tailed lemur (Lemur catta). The shoulder muscles (supraspinatus, infraspinatus, teres major, teres minor, and subscapularis) were embedded in celloidin and cut into transverse serial thin sections (40 microm); then, every tenth section was stained using the Azan staining technique. The relative muscle weights and the density of the muscle spindles were determined. The slow loris muscles were heavier and had sparser muscle spindles, as compared to Garnett's galago. These features suggest that the shoulder muscles of the slow loris are more adapted to generating propulsive force and stabilizing the shoulder joint during locomotion and play a less controlling role in forelimb movements. In contrast, Garnett's galago possessed smaller shoulder muscles with denser spindles that are suitable for the control of more rapid locomotor movements. The mean relative weight and the mean spindle density in the shoulder muscles of the ring-tailed lemur were between those of the other primates, suggesting that the spindle density is not simply a consequence of taxonomic status.

Do highly trained monkeys walk like humans? A kinematic study of bipedal locomotion in bipedally trained Japanese macaques.

In this study, we examined the kinematics of bipedal walking in macaque monkeys that have been highly trained to stand and walk bipedally, and compared them to the kinematics of bipedal walking in ordinary macaques. The results revealed that the trained macaques walked with longer and less frequent strides than ordinary subjects. In addition, they appear to have used inverted pendulum mechanics during bipedal walking, which resulted in an efficient exchange of potential and kinetic energy. These gait characteristics resulted from the relatively more extended hindlimb joints of the trained macaques. By contrast, the body of the ordinary macaques translated downward during the single-limb stance phase due to more flexed hindlimb joints. This resulted in almost in-phase fluctuations of potential and kinetic energy, which indicated that energy transformation was less efficient in the ordinary macaques. The findings provide two insights into the early stage of the evolution of human bipedalism. First, the finding that training considerably improved bipedal walking a posteriori may explain why the very first bipeds that might not yet have been morphologically adapted to bipedal walking continued to walk bipedally. The evolutionary transition from quadrupedalism to bipedalism might not be as difficult as has been envisioned. In addition, the finding that macaques, which are phylogenetically distant from humans and in which bipedal walking is unlike human walking, could develop humanlike gait characteristics with training, provides strong support for the commonly held but unproven idea that the characteristics of the human gait are advantageous to human bipedalism.

Head movements during locomotion in a gibbon and Japanese macaques.

Kinematic analysis of head and body movements during locomotion in Macaca fuscata and Hylobates lar revealed that coordinated head rotation and translation that have been reported to play an important role in stabilizing gaze during locomotion for humans are also observed in non-human primates. The fact that well-coordinated head movements were observed in two species, and during both bipedal and quadrupedal walking, suggests that the head orientation during locomotion is well regulated in the manner of top-down control over the species and modes of locomotion. The result validates the monkey model and enables us to explore the underlying mechanisms for gaze, head, and postural control during locomotion.