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.     

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.     

Effect of posture and locomotion on energy expenditure

Energy expenditure for human adults and infants and for dogs was measured in resting (supine or lateral) posture, in bipedal posture and locomotion, and in quadrupedal posture and locomotion. Variations in respiratory and heart rate and in body temperature were utilized in this comparative study. Oxygen consumption was also measured in human adults. In human adults, bipedal posture and locomotion were shown to be much less energy-consuming than corresponding quadrupedal posture and locomotion. The opposite was observed in adult dogs, where bipedalism was shown to be much more energy-consuming than quadrupedalism. In addition, this study demonstrated, for human adults in their natural erect posture, an energy expenditure barely higher than in supine or lateral resting posture, while the dogs in their natural quadrupedal stance, the energy expenditure is much higher than in their resting posture. With respect to energy, therefore, humans are more adapted to bipedalism than dogs to quadrupedalism. Human children, at the transitional stage between quadrupedalism and bipedalism, have high and almost equal requirements for all postures and locomotions. This demonstrates, in term of energy, their incomplete adaptation to erect behavior.     

Comparative and functional anatomy of phalanges in<Emphasis Type="Italic"> Nacholapithecus kerioi</Emphasis>, a Middle Miocene hominoid from northern Kenya

We describe phalanges of the KNM-BG 35250 Nacholapithecus kerioi skeleton from the Middle Miocene of Kenya. Phalanges of N. kerioi display similarities to those of Proconsul heseloni despite their enhanced robusticity. They do not show highly specialized features as in living suspensory primates. However, N. kerioi manifests several distinctive features that are observed in neither living arboreal quadrupeds nor P. heseloni or P. nyanzae. The most remarkable of them is its phalangeal elongation. N. kerioi phalanges (particularly pedal) are as long as those of Pan despite its much smaller body size. While lengthened digits enable a secure grip of supports and are especially adaptive for grasping large vertical trunks, the skeletal and soft tissues are subjected to greater stress. Probably, strong selective pressures favored powerful hallucal/pollical assisted grips. Although this functional adaptation does not exclude the possible use of the terrestrial environment, arboreal behavioral modes must have been crucial in its positional repertoire. N. kerioi is distinguished from P. heseloni in the greater size of its manual phalanges over its pedal phalanges. These derived features of N. kerioi suggest positional modes supporting more weight on the forelimb, and which occur more frequently on vertical supports. If Proconsul is referred to as an "above-branch arboreal quadruped" with a deliberate and effective climbing capability, N. kerioi may be thought of as an "orthograde climber". While living apes are powerful orthograde climbers, they are also more or less suspensory specialists. Suspensory behavior (plus climbing) and pronograde quadrupedalism (plus climbing) are the two main arboreal behavioral adaptations in living anthropoids. Thus, N. kerioi is an unusual fossil primate in that it cannot be incorporated into this dichotomy. It is plausible that a N. kerioi-like orthograde climber with large forelimbs and cheiridia was a precursor of suspensory living apes, and N. kerioi may demonstrate what an initial hominoid of this grade might have looked like.     

Serratus ventralis function in vervet monkeys (Cercopithecus aethiops): are primate quadrupeds unique?

The serratus ventralis in mammals is a fan-shaped scapulo-thoracic muscle that is believed by most morphologists both to support body weight and to rotate the scapula during quadrupedal locomotion. Electromyographic studies of this muscle in cats, dogs and opossums confirm the dual supportive and rotatory roles of the serratus ventralis. Although this muscle has been studied in several primate species, the concentration on arboreal locomotion has resulted in an inadequate data set to permit direct comparisons to non-primate terrestrial quadrupeds. In order to provide a more comparable data set, we examined cranial, mid- and caudal thoracic regions of the serratus ventralis during terrestrial quadrupedalism in the vervet monkey, Cereopithecus aethiops. Our results indicate that the serratus ventralis does support the body during the stance phase of quadrupedalism in this primate. However, unlike several non-primate mammals, it plays a relatively insignificant rotatory role during swing phase.     

Bioenergetics and the origin of hominid bipedalism

Compared to most quadrupedal mammals, humans are energetically inefficient when running at high speeds. This fact can be taken to mean that human bipedalism evolved for reasons other than to reduce relative energy cost during locomotion. Recalculation of the energy expended during human walking at normal speeds shows that (1) human bipedalism is at least as efficient as typical mammalian quadrupedalism and (2) human gait is much more efficient than bipedal or quadrupedal locomotion in the chimpanzee. We conclude that bipedalism bestowed an energetic advantage on the Miocene hominoid ancestors of the Hominidae.     

Locomotion and palaeoclimate explain the re-evolution of quadrupedal body form in Brachymeles lizards

Evolutionary reversals, including re-evolution of lost structures, are commonly found in phylogenetic studies. However, we lack an understanding of how these reversals happen mechanistically. A snake-like body form has evolved many times in vertebrates, and occasionally a quadrupedal form has re-evolved, including in Brachymeles lizards. We use body form and locomotion data for species ranging from snake-like to quadrupedal to address how a quadrupedal form could re-evolve. We show that large, quadrupedal species are faster at burying and surface locomotion than snake-like species, indicating a lack of expected performance trade-off between these modes of locomotion. Species with limbs use them while burying, suggesting that limbs are useful for burying in wet, packed substrates. Palaeoclimatological data suggest that Brachymeles originally evolved a snake-like form under a drier climate probably with looser soil in which it was easier to dig. The quadrupedal clade evolved as the climate became humid, where limbs and large size facilitated fossorial locomotion in packed soils.     

Electromyography of back muscles during quadrupedal and bipedal walking in primates

Despite the extensive electromyographic research that has addressed limb muscle function during primate quadrupedalism, the role of the back muscles in this locomotor behavior has remained undocumented. We report here the results of an electromyographic (EMG) analysis of three intrinsic back muscles (multifidus, longissimus, and iliocostalis) in the baboon (Papio anubis), chimpanzee (Pan troglodytes), and orangutan (Pongo pygmaeus) during quadrupedal walking. The recruitment patterns of these three back muscles are compared to those reported for the same muscles during nonprimate quadrupedalism. In addition, the function of the back muscles during quadrupedalism and bipedalism in the two hominoids is compared. Results indicate that the back muscles restrict trunk movements during quadrupedalism by contracting with the touchdown of one or both feet, with more consistent activity associated with touchdown of the contralateral foot. Moreover, despite reported differences in their gait preferences and forelimb muscle EMG patterns, primates and nonprimate mammals recruit their back muscles in an essentially similar fashion during quadrupedal walking. These quadrupedal EMG patterns also resemble those reported for chimpanzees, gibbons and humans (but not orangutans) walking bipedally. The fundamental similarity in back muscle function across species and locomotor behaviors is consistent with other data pointing to conservatism in the evolution of the neural control of tetrapod limb movement, but does not preclude the suggestion (based on forelimb muscle EMG and spinal lesion studies) that some aspects of primate neural circuitry are unique. © 1994 Wiley-Liss, Inc.     

Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus)

We collected high-resolution plantar pressure distributions of seven bonobos during terrestrial bipedal and quadrupedal locomotion (N = 146). Functional foot length, degree of hallux abduction, and total contact time were determined, and plots, showing pressure as a function of time for six different foot regions, were generated. We also studied five adult humans for comparison (N = 13). Both locomotion types of the bonobo show a large variation in plantar pressure distributions, which could be due to the interference of instantaneous behavior with locomotion and differences in walking speed and body dimensions. The heel and the lateral midfoot typically touch down simultaneously at initial ground contact in bipedal and quadrupedal walking of bonobos, in contrast with the typical heel-strike of human bipedalism. The center of pressure follows a curved course during quadrupedalism, as a consequence of the medial weight transfer during mid-stance. Bipedal locomotion of bonobos is characterized by a more plantar positioning of the feet and by a shorter contact time than during quadrupedal walking, according to a smaller stride and step length at a higher frequency. We observed a varus position of the foot with an abducted hallux, which likely possesses an important sustaining and stabilizing function during terrestrial locomotion.     

Human Quadrupeds,Primate Quadrupedalism,and Uner Tan Syndrome

Since 2005, an extensive literature documents individuals from several families afflicted with “Uner Tan Syndrome (UTS),” a condition that in its most extreme form is characterized by cerebellar hypoplasia, loss of balance and coordination, impaired cognitive abilities, and habitual quadrupedal gait on hands and feet. Some researchers have interpreted habitual use of quadrupedalism by these individuals from an evolutionary perspective, suggesting that it represents an atavistic expression of our quadrupedal primate ancestry or “devolution.” In support of this idea, individuals with “UTS” are said to use diagonal sequence quadrupedalism, a type of quadrupedal gait that distinguishes primates from most other mammals. Although the use of primate-like quadrupedal gait in humans would not be sufficient to support the conclusion of evolutionary “reversal,” no quantitative gait analyses were presented to support this claim. Using standard gait analysis of 518 quadrupedal strides from video sequences of individuals with “UTS”, we found that these humans almost exclusively used lateral sequence–not diagonal sequence–quadrupedal gaits. The quadrupedal gait of these individuals has therefore been erroneously described as primate-like, further weakening the “devolution” hypothesis. In fact, the quadrupedalism exhibited by individuals with UTS resembles that of healthy adult humans asked to walk quadrupedally in an experimental setting. We conclude that quadrupedalism in healthy adults or those with a physical disability can be explained using biomechanical principles rather than evolutionary assumptions.     

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.     

EMG of chimpanzee shoulder muscles during knuckle-walking: problems of terrestrial locomotion in a suspensory adapted primate

By most accounts, the upper limb of the chimpanzee is primarily adapted to suspensory postures and locomotion. In order to determine how the derived morphology of the chimpanzee forelimb has affected the form of quadrupedal locomotion displayed by these animals, electromyographic activity patterns of 10 shoulder muscles during knuckle-walking in two chimpanzee subjects were analysed and compared to data on the opossum and cat taken from the literature. Telemetered electromyography coupled with simultaneous video recording was employed in order to study unfettered locomotion in the chimpanzee subjects.
Chimpanzees are characterized by a quadrupedal gait in which the hind limb overstrides the ipsilateral forelimb. Forelimb position in the plane of abduction/adduction is significantly affected by whether the hind limb passes inside or outside its ipsilateral forelimb. The degree of abduction adduction of the forelimb, in turn, influences many of the muscle activity patterns. That is, some muscles would be more frequently or less frequently active, depending on whether the arm was relatively abducted or adducted during a stride. Thus, there can be no single motor programme that generates the step cycle in chimpanzees.
While there are some parallels between muscle recruitment patterns for chimpanzee, opossum and cat quadrupedalism, the results of this study also indicate that many aspects of muscle use in chimpanzees have been significantly influenced by factors related to increased mobility of the upper limb. Finally, this study has revealed that moving the arm forward during swing phase of knuckle-walking is not a simple product of muscular elTort. and that other mechanisms must be involved. However, it is unclear at present exactly what these mechanisms may be.     

Locomotor and postural behavior in Alouatta palliata and Cebus capucinus

Positional behavior of two platyrrhine monkeys, Alouatta palliata and Cebus capucinus, was observed at La Pacifica and Santa Rosa National Park, Costa Rica. Frequency data for locomotion, postures, support diameters, orientation of supports, and use of canopy were recorded on focal males and females. Alouatta palliata is a frequent user of arboreal quadrupedalism (47%) and climbing (37%), with bridging (10%) representing the next most frequent type of locomotion. Intraspecific comparisons show the smaller-sized females of Alouatta to prefer very small diameter supports, the lower canopy, and to climb more frequently than the larger males—a pattern opposite to that which has been documented to occur with increasing body size across species. A more limited study on Cebus capucinus shows this species to be highly quadrupedal (54%) with moderately high locomotor frequencies for climbing (26%) and leaping (15%).     

Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates

The forelimb joints of terrestrial primate quadrupeds appear better able to resist mediolateral (ML) shear forces than those of arboreal quadrupedal monkeys. These differences in forelimb morphology have been used extensively to infer locomotor behavior in extinct primate quadrupeds. However, the nature of ML substrate reaction forces (SRF) during arboreal and terrestrial quadrupedalism in primates is not known. This study documents ML-SRF magnitude and orientation and forelimb joint angles in six quadrupedal anthropoid species walking across a force platform attached to terrestrial (wooden runway) and arboreal supports (raised horizontal poles). On the ground all subjects applied a lateral force in more than 50% of the steps collected. On horizontal poles, in contrast, all subjects applied a medially directed force to the substrate in more than 75% of the steps collected. In addition, all subjects on arboreal supports combined a lower magnitude peak ML-SRF with a change in the timing of the ML-SRF peak force. As a result, during quadrupedalism on the poles the overall SRF resultant was relatively lower than it was on the runway. Most subjects in this study adduct their humerus while on the poles. The kinetic and kinematic variables combine to minimize the tendency to collapse or translate forelimbs joints in an ML plane in primarily arboreal quadrupedal primates compared to primarily terrestrial quadrupedal ones. These data allow for a more complete understanding of the anatomy of the forelimb in terrestrial vs. arboreal quadrupedal primates. A better understanding of the mechanical basis of morphological differences allows greater confidence in inferences concerning the locomotion of extinct primate quadrupeds.     

Further evidence for the role of supraspinatus in quadrupedal monkeys.

Differences in the degree of projection of the greater tubercle above the level of the humeral head in primate proximal humeri have been associated with differing leverage requirements for supraspinatus during arboreal vs. terrestrial quadrupedal locomotion. Since most workers have assumed that supraspinatus acts as a humeral protractor, interpretations of the variation in greater tubercle height have focused on the need for powerful vs. rapid humeral protraction during the swing phase of quadrupedal locomotion. However, in an EMG study on the activity patterns of supraspinatus in the vervet monkey, Larson and Stern (Am. J. Phys. Anthropol. 79:369-377, 1989) reported that although supraspinatus is active during arm elevations against gravity, it is silent during the swing phase of quadrupedal locomotion, and instead acts as a joint stabilizer during support phase. They suggested that the pattern of activity for supraspinatus observed in the vervet was common for all quadrupedal primates, and that differences in greater tubercle projection could be related to the degree of mobility of the shoulder. In the current study, we present additional EMG data on a baboon and three macaques supporting the suggestions offered by Larson and Stern (1989).     

Comparative postcranial body shape and locomotion in Chlorocebus aethiops and Cercopithecus mitis

Body weight and length, chest girth, and seven postcranial limb segment lengths are compared between two guenon species, Chlorocebus (Cercopithecus) aethiops (vervets) and Cercopithecus mitis (blue monkeys), exhibiting different habitual locomotor preferences. The subjects, all adults, were wild caught for a non-related research project (Turner et al. [1986] Genetic and morphological studies on two species of Kenyan monkeys, C. aethiops and C. mitis. In: Else JG, Lee PC, editors. Primate evolution, proceedings of the Xth International Congress of Primatology, Cambridge. London). The morphological results are interpreted within the context of previously published observations of primate locomotion and social organization. The sample is unique in that the body weight of each individual is known, allowing the effects of body-size scaling to be assessed in interspecific and intersexual comparisons. C. mitis has a significantly (P < 0.05) greater body weight and trunk length than C. aethiops. A shorter trunk may function to reduce spinal flexibility for ground-running in the latter. Proximal limb segments (arm and thigh) are significantly greater in C. mitis, reflecting known adaptations to committed arboreal quadrupedal locomotion. By contrast, relative distal limb segments (forearm, crus, and foot) are significantly longer in C. aethiops, concordant with a locomotor repertoire that includes substantial terrestrial quadrupedalism, in addition to arboreal agility, and also the requisite transition between ground and canopy. Although normally associated with arboreal monkeys, greater relative tail length occurs in the more terrestrial vervets. However, because vervets exploit both arboreal and terrestrial habitats, a longer tail may compensate for diminished balance during arboreal quadrupedalism resulting from the greater "brachial" and "crural" indices that enhance their ground quadrupedalism. Most interspecific differences in body proportions are explicable by differences in locomotor modalities. Some results, however, contradict commonly held "tenets" that relate body size and morphology exclusively to locomotion. Generally associated with terrestriality, sexual dimorphism (male/female) is greater in the more arboreal blue monkeys. A more intense, seasonal mating competition may account for this incongruity.     

Variations in blood supply allocations for quadrupedal and for bipedal posture and locomotion

Hemodynamics and orthodynamics were investigated in quadrupeds (dogs) and in bipeds (humans). The subjects were investigated at rest in supine or lateral posture, in quadrupedal and then in bipedal posture, and during locomotion. Quadrupedalism in humans was with subjects on their hands and knees. Bipedalism in dogs was on hindlimbs with the forelimbs held by a technician. Blood flow in the main arteries of the body (aorta, external and internal carotid, subclavian, and femoral) was measured by sonography. Positional variations between the main bones of the body were determined from X-rays. This study investigated the reallocation of blood supply to different regions of the body when it switches from quadrupedal to bipedal posture and locomotion. Compared with resting posture, the principal findings are 1) cardiac output shows a minimal increase for humans in bipedal stance and a noticeable increase for dogs as well as humans in quadrupedal stance; 2) quadrupedal stance in humans and dogs and bipedal stance in dogs require increased blood supply to the muscles of the neck, back, and limbs, while human bipedal stance requires none of these; 3) cerebral blood flow (internal carotid) in humans did not change as a result of bipedal posture or locomotion, but showed a noticeable drop in quadrupedal posture and an even further drop in quadrupedal locomotion. The conclusion is that erect posture and encephalization produced a noticeable readjustment and reallocation of blood flow among the different regions of the body: This consisted in shifting a large volume of blood supply from the musculature to the human brain.     

广西西南部石山森林中熊猴的姿势行为

灵长类动物姿势行为研究对了解其环境适应机制具有重要意义.2012年9月至2013年8月,采用瞬时扫描取样法对广西弄岗国家级自然保护区内一群熊猴(Macaca assamensis)的姿势行为进行观察,比较熊猴姿势行为的季节和日时段变化.结果 表明,熊猴移动模式的频率存在显著差异,从高到低为四足行走(45.3％±7.6％...     

Energy expenditure of bipedal walking is higher than that of quadrupedal walking in Japanese macaques

The authors previously compared energetic costs of bipedal and quadrupedal walking in bipedally trained macaques used for traditional Japanese monkey performances (Nakatsukasa et al. 2004 Am. J. Phys. Anthropol. 124:248-256). These macaques used inverted pendulum mechanics during bipedal walking, which resulted in an efficient exchange of potential and kinetic energy. Nonetheless, energy expenditure during bipedal walking was significantly higher than that of quadrupedal walking. In Nakatsukasa et al. (2004 Am. J. Phys. Anthropol. 124:248-256), locomotor costs were measured before subjects reached a steady state due to technical limitations. The present investigation reports sequential changes of energy consumption during 15 min of walking in two trained macaques, using carbon dioxide production as a proxy of energy consumption, as in Nakatsukasa et al. (2004 Am. J. Phys. Anthropol. 124:248-256). Although a limited number of sessions were conducted, carbon dioxide production was consistently greater during bipedal walking, with the exception of some irregularity during the first minute. Carbon dioxide production gradually decreased after 1 min, and both subjects reached a steady state within 10 min. Energy expenditure during bipedalism relative to quadrupedalism differed between the two subjects. It was considerably higher (140% of the quadrupedal walking cost) in one subject who walked with more bent-knee, bent-hip gaits. This high cost strongly suggests that ordinary macaques, who adopt further bent-knee, bent-hip gaits, consume a far greater magnitude of energy during bipedal walking.