Inefficient use of inverted pendulum mechanism during quadrupedal walking in the Japanese macaque

In animal walking, the gravitational potential and kinetic energy of the center of mass (COM) fluctuates out-of-phase to reduce the energetic cost of locomotion via an inverted pendulum mechanism, and, in canine quadrupedal walking, up to 70% of the mechanical energy can be recovered. However, the rate of energy recovery for quadrupedal walking in primates has been reported to be comparatively lower. The present study analyzed fluctuations in the potential and kinetic energy of the COM during quadrupedal walking in the Japanese macaque to clarify the mechanisms underlying this inefficient utilization of the inverted pendulum mechanism in primates. Monkeys walked on a wooden walkway at a self-selected speed, and ground reaction forces were measured, using a force platform, to calculate patterns of mechanical energy fluctuation and rates of energy recovery. Our results demonstrated that rates of energy recovery for quadrupedal walking in Japanese macaques were approximately 30–50%, much smaller than those reported for dogs. Comparisons of the patterns of mechanical energy fluctuation suggested that the potential and kinetic energies oscillated relatively more in-phase, and amplitudes did not attain near equality during quadrupedal walking in Japanese macaques, possibly because of greater weight support (reaction force) of the hindlimbs and more protracted forelimbs at touchdown in the Japanese macaque, two of the three commonly accepted locomotor characteristics distinguishing primates from non-primate mammals.     

Biomechanical analysis of vertical climbing in the spider monkey and the Japanese macaque

Climbing is one of the most important components of primate locomotor modes. We previously reported that the kinesiological characteristics of vertical climbing by the spider monkey and Japanese macaque are clearly different, based on their kinetics and kinematics. In this study, a more detailed analysis using inverse dynamics was conducted to estimate the biomechanical characteristics of vertical climbing in the spider monkey and Japanese macaque. One of the main findings was the difference in forelimb use by the two species. The results of a joint moment analysis and estimates of muscular force indicate that the spider monkey uses its forelimbs to keep the body close to the substrate, rather than to generate propulsion. The forelimb of the Japanese macaque, on the other hand, likely contributes more to propulsion. This supports the idea that "forelimb-hindlimb differentiation" is promoted in the spider monkey. The estimated muscular force also suggests that the spider monkey type of climbing could develop the hindlimb extensor muscles, which are important in bipedal posture and walking. As a result, we conclude that the spider monkey type of climbing could be functionally preadaptive for human bipedalism. This type of climbing would develop the hip and knee extensor muscles, and result in more extended lower limb joints, a more erect trunk posture, and more functionally differentiated fore- and hindlimbs, all of which are important characteristics of human bipedalism.     

Interpreting the Role of Climbing in Primate Locomotor Evolution: Are the Biomechanics of Climbing Influenced by Habitual Substrate Use and Anatomy?

Vertical climbing is widely accepted to have played an important role in the origins of both primate locomotion and of human bipedalism. Yet, only a few researchers have compared climbing mechanics in quadrupedal primates that vary in their degree of arboreality. It is assumed that primates using vertical climbing with a relatively high frequency will have morphological and behavioral specializations that facilitate efficient climbing mechanics. We test this assumption by examining whether time spent habitually engaged in climbing influences locomotor parameters such as footfall sequence, peak forces, and joint excursions during vertical climbing. Previous studies have shown that during climbing, the pronograde and semiterrestrial Macaca fuscata differs in these parameters compared to the more arboreal and highly specialized, antipronograde Ateles geoffroyi. Here, we examine whether a fully arboreal, quadrupedal primate that does not regularly arm-swing will exhibit gait and force distribution patterns intermediate between those of Macaca fuscata and Ateles geoffroyi. We collected footfall sequence, limb peak vertical forces, and 3D hindlimb excursion data for Macaca fascicularis during climbing on a stationary pole instrumented with a force transducer. Results show that footfall sequences are similar between macaque species, whereas peak force distributions and hindlimb excursions for Macaca fascicularis are intermediate between values reported for M. fuscata and Ateles geoffroyi. These results support the notion that time spent climbing is reflected in climbing mechanics, even though morphology may not provide for efficient mechanics, and highlight the important role of arboreal locomotor activity in determining the pathways of primate locomotor evolution.     

Locomotion in captive Leontopithecus and Callimico: A multimedia study

Video studies, gait analysis, footprint tracks, and observational scan sampling show that, in comparably furnished enclosures, Leontopithecus rosalia and Callimico goeldii are superficially similar in their use of predefined locomotor patterns but differ profoundly in many underlying details which reflect differences in postcranial morphology. Each uses pronograde arboreal quadrupedal walking, quadrupedal bounding, and vertical climbing with comparable frequency, and both shift to bounding while moving quadrupedally at high speeds. In walking, both species use a diagonal sequence gait. However, in Callimico the distance per bout traveled while walking or running is shorter than in L. rosalia and there is an emphasis on leaping (from a stationary position) and bounding-leaps (saltational extensions of pronograde quadrupedalism), in contrast with the basically quadrupedal style of L. rosalia. This dichotomy is consistent with anatomical specializations, such as forelimb elongation in Leontopithecus and hindlimb elongation in Callimico. In vivo hand- and footprint studies demonstrate grasping halluces in both species while walking. Limb stances in L. rosalia during “transaxial bounding” involve an overstriding hindlimb, a predominance of oblique rather than in-line travel, and unique hand and foot positions. Anatomically, this locomotor style may be associated with reduced dexterity of the elongate hands and a relatively short hallux. The captive locomotor profiles for both species probably reflect biased samples of the locomotor repertoire of their wild counterparts. Nevertheless, these data reflect species-specific integrations of locomotor behavior and morphology, and corroborate expectations of locomotor diversity among callitrichine primates, even those of similar body size. It is suggested, however, that conventional quantitative studies of locomotor profiles may prove inadequate for resolving subtle aspects of locomotor morphology and behavior. © 1994 Wiley-Liss, Inc.     

Hindlimb dominance during primate high-speed locomotion

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.     

Forward dynamic simulation of bipedal walking in the Japanese macaque: investigation of causal relationships among limb kinematics, speed, and energetics of bipedal locomotion in a nonhuman primate

Japanese macaques that have been trained for monkey performances exhibit a remarkable ability to walk bipedally. In this study, we dynamically reconstructed bipedal walking of the Japanese macaque to investigate causal relationships among limb kinematics, speed, and energetics, with a view to understanding the mechanisms underlying the evolution of human bipedalism. We constructed a two-dimensional macaque musculoskeletal model consisting of nine rigid links and eight principal muscles. To generate locomotion, we used a trajectory-tracking control law, the reference trajectories of which were obtained experimentally. Using this framework, we evaluated the effects of changes in cycle duration and gait kinematics on locomotor efficiency. The energetic cost of locomotion was estimated based on the calculation of mechanical energy generated by muscles. Our results demonstrated that the mass-specific metabolic cost of transport decreased as speed increased in bipedal walking of the Japanese macaque. Furthermore, the cost of transport in bipedal walking was reduced when vertical displacement of the hip joint was virtually modified in the simulation to be more humanlike. Human vertical fluctuations in the body's center of mass actually contributed to energy savings via an inverted pendulum mechanism.     

Energetic costs of bipedal and quadrupedal walking in Japanese macaques

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 quadrupedal 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.     

Comparative locomotion of six sympatric primates in Ecuador

Primates exhibit a great variety of arboreal locomotor modes associated with their size and postcranial morphology. The study of sympatric primates is interesting in that it may reveal how primates of different sizes and anatomies move and select for forest structure. This study reports on preliminary data on the locomotion of six non-ateline platyrrhines found in the Yasuni National Park, Napo Province, Ecuador. Pygmy marmosets are confined to the understory using scansorial locomotion and quadrupedalism, preferring large vertical supports. Golden-mantled tamarins, common squirrel monkeys and dusky titis also range in the understory, moving by quadrupedal walk and leap, mainly on small horizontal supports. Monk sakis are found in the main canopy and use quadrupedal walk and less leap on medium-sized horizontal supports. Whitefronted capuchins use the understory and the main canopy equally often, walking quadrupedally and leaping on small and medium-sized oblique supports. In general, smaller species occupy lower strata while larger species tend to spend more time in the upper strata. Small tegulae-bearing monkeys showed the highest proportions of large vertical support use. For all species, leaping was the main gap-crossing mode, though decreasing in proportion with a higher use of the upper forest layers.     

Preliminary electromyographical analysis of brachiation in gibbon and spider monkey

In order to refine the concept of brachiation as a locomotor mode and to examine the complex relationship between locomotor behavior and muscle morphology, we have undertaken a telemetered electromyographic (EMG) analysis of muscle recruitment in brachiating gibbons (Hylobates lar) and spider monkeys (Ateles belzebuth andAteles fusciceps) Electrical activity patterns were determined for both support and swing phases in the following muscles: cranial pectoralis major, caudal pectoralis major, middle deltoideus, short head of biceps brachii, flexor digitorum superficialis, latissimus dorsi, and dorsoepitrochlearis. Our experimental findings reinforce earlier behavioral observations that brachiation is not a discrete, stereotyped locomotor activity. EMG patterns differed most between gibbon and spider monkey in those muscles that exhibit markedly disparate morphologies in the two genera-pectoralis major (both portions) and the short head of biceps brachii. Additional recruitment differences appear related to consistent species-specific differences in the timing and mechanics of both support and swing phases, and probably to the role of the prehensile tail as a fail-safe mechanism in the spider monkey.     

Origin of bipedalism

Human and chimpanzee locomotor behaviors are described and compared using field patterns derived from measurements of the motions at the joints. Field patterns of human and ape bipedalism are so different that it is doubted whether the nonhuman type could ever have been a precursor of the human type. Chimpanzee quadrupedal vertical climbing and human bipedalism are, on the other hand, similar and a particular variety of this kind of climbing probably was the precursor of human bipedalism. Animals adapted to this variation would have had some brachiation-like morphological traits in their pectoral limbs and some hominid-like morphological traits in their pelvic limbs, traits anticipating the human condition. The australopithecines possessed these traits and must have been adapted to arboreal quadrupedal vertical climbing, having the capacity, at the same time, to perform facultative terrestrial bipedalism, moving on the ground in a manner visually identical to that of humans.     

Optimization of the mechanical performance of a two-duct semicircular duct system--part 3: the positioning of the ducts in the head

In the majority of vertebrates, the horizontal duct of the vestibular system lies approximately in the yawing plane of the head. The positioning of the vertical ducts, however, is not in the pitch- and roll planes but the vertical ducts generally lie under an angle of about 30-45 degrees relative to the medial plane. Using the equations for a hydrodynamically interconnected two-duct system, optimal positions of the vertical and horizontal ducts in different vertebrate groups can be derived. It was stated that the mean response of the vertical ducts should be optimized. This leads to a symmetrical positioning of the vertical ducts with respect to the medial plane. In all observed vertebrate groups, a solution of mu =(pi-alpha)/2 is found (mu is the angle of the vertical ducts relative to the medial plane, alpha is the angle between the vertical duct planes). For alpha=90 degrees, this provides an equal sensitivity for pitch- and roll- movements. For alpha>90 degrees, a larger sensitivity for pitch movements is obtained, at the expense of a lower sensitivity for roll movements. It is argued that the angle alpha between the vertical ducts may vary from 90 to 120 degrees. In most vertebrates, the centre of mass is stabilized by e.g. fins, tri- or quadrupedal stability, a crawling body or upside-down resting positions (e.g. bats). Birds are generally biped, so in walking they are also rather sensitive to roll. These features are related to labyrinth positioning in the head.     

Origins of primate locomotion: gait mechanics of the woolly opossum

The locomotion of primates differs from that of other mammals in three fundamental ways. During quadrupedal walking, primates use diagonal sequence gaits, protract their arms more at forelimb touchdown, and experience lower vertical substrate reaction forces on their forelimbs relative to their hindlimbs. It is widely held that the unusual walking gaits of primates represent a basal adaptation for movement on thin, flexible branches and reflect a major change in the functional role of the forelimb. However, little data on nonprimate arboreal mammals exist to test this notion. To that end, we examined the gait mechanics of the woolly opossum (Caluromys philander), a marsupial convergent with small-bodied prosimians in ecology, behavior, and morphology. Data on the footfall sequence, relative arm protraction, and peak vertical substrate reaction forces were obtained from videotapes and force records for three adult woolly opossums walking quadrupedally on a wooden runway and a thin pole. For all steps recorded on both substrates, woolly opossums always used diagonal sequence walking gaits, protracted their arms beyond 90 degrees relative to horizontal body axis, and experienced peak vertical substrate reaction forces on forelimbs that were significantly lower than on hindlimbs. The woolly opossum is the first nonprimate mammal to show locomotor mechanics that are identical to those of primates. This case of convergence between primates and a committed fine-branch, arboreal marsupial strongly implies that the earliest primates evolved gait specializations for fine-branch locomotion, which reflect important changes in forelimb function.     

Positional behavior of long-tailed macaques (Macaca fascicularis) in northern Sumatra

Although the majority of extant primates are described as "quadrupedal," there is little information available from natural habitats on the locomotor and postural behavior of arboreal primate quadrupeds that are not specialized for leaping. To clarify varieties of quadrupedal movement, a quantitative field study of the positional behavior of a highly arboreal cercopithecine, Macaca fascicularis, was conducted in northern Sumatra. At least 70% of locomotion in travel, foraging, and feeding was movement along continuous substrates by quadrupedalism and vertical climbing. Another 14-25% of locomotion was across substrates by pronograde clambering and vertical clambering. The highest frequency of clambering occurred in foraging for insects, and on the average smaller substrates were used in clambering than during quadrupedal movement. All postural behavior during foraging and feeding was above-substrate, largely sitting. Locomotion across substrates requires grasping branches of diverse orientations, sometimes displaced away from the animal's body. The relatively low frequency of across-substrate locomotion appears consistent with published analyses of cercopithecoid postcranial morphology, indicating specialization for stability of limb joints and use of limbs in parasagittal movements, but confirmation of this association awaits interspecific comparisons that make the distinction between along- and across-substrate forms of locomotion. It is suggested that pronograde clambering as defined in this study was likely a positional mode of considerable importance in the repertoire of Proconsul africanus and is a plausible early stage in the evolution of later hominoid morphology and locomotor behavior.     

Locomotion and posture in Lagothrix lagotricha

This long-term study of woolly monkey (Lagothrix) locomotor and postural behaviour employs methods identical to those used during a previous study of the locomotion and posture of two species of Ateles, allowing a detailed comparison between the two genera, which are strong competitors in extensive parts of the Amazon basin and northern Andes. As in Ateles, Lagothrix locomotion can be divided into five patterns, based on limb usage: quadrupedal walking and running, suspensory locomotion, climbing, bipedalism (very rare in wild woolly monkeys) and leaping. Lagothrix differs from Ateles primarily in its greater reliance on quadrupedal locomotion during both travel and feeding and on its de-emphasis of the use of suspensory locomotion as compared to Ateles, while the use of climbing and leaping is roughly equal in the two genera. Lagothrix exhibits more generalised (primitive) locomotive behaviour in accordance with its morphology, in comparison to the more specialised Ateles. The generic differences reflect differences in habitat use and particularly foraging ecology.     

The locomotor and postural repertoires of Ateles geoffroyi and Colobus guereza,and a reevaluation of the locomotor category semibrachiation

The locomotor repertoire of Ateles geoffroyi includes quadrupedal walking and running, climbing, brachiation and arm-swinging, bipedalism, and leaping. Its postural repertoire is characterized by below branch suspensory activities. In contrast, the locomotor repertoire of Colobus guereza consists primarily of quadrupedal galloping and bounding, and leaping. It does not brachiate or walk bipedally and rarely performs arm-swinging. The Colobus guereza postural repertoire is characterized by above branch sitting postures. Ateles geoffroyi is a highly mobile primate, whereas Colobus guereza is essentially sedentary. In the past, there has been a tendency to group Ateles and Colobus in a single locomotor category, semibrachiation. Comparison of the very different repertoires of these two species points out some of the shortcomings of the category semibrachiation. First, no locomotor pattern or group of patterns has been described as semibrachiation (i.e., no animals semibrachiate). Secondly, the locomotor diversity of animals included in the category is so much greater than the similarities that the category obscures more than it conveys. The usefulness of retaining this category is therefore questioned.     

Primates in perspective. Review of “Order Primates,” pp. 352–450 in Walker's Mammals of the World, 4th Edition,by Ronald M. Nowak and John L. Paradiso. Baltimore and London,The Johns Hopkins University Press, 1983, 1362 pp., two-volume set, $65

This study examines the positional and activity behavior of a captive slow loris, Nycticebus coucang. The male individual was housed in a primate facility providing a seminatural environment and was subjected to a series of videotape recordings from which 1,878 point observations were taken. The enclosure was designed to allow maximum flexibility of substrate use. Quantitative information detailing activity, positional mode, and substrate geometry was collected using a checklist of 15 variables. Data were tabulated and compared as frequency distributions to describe activity budgets, the use of locomotor and postural modes, and the relation of posture to activity behavior and substrate geometry. The results indicated that almost 90% of the active day may be devoted to behaviors directly or indirectly related to dietary functions. For locomotor behavior, both climbing and walking were associated with the use of diagonal couplets. The loris devoted 52% of its positional behavior to postural modes, favoring the quadrupedal stand, triplets, and sitting. Suspension was found to be used more often in posture than locomotion. Overall, the loris's repertory of positional modes accommodated a wide range of substrate geometries.