Symmetrical gaits of Cebus apella: implications for the functional significance of diagonal sequence gait in primates

Quadrupedal locomotion of primates is distinguished from the quadrupedalism of many other mammals by several features, including a diagonal sequence (DS) footfall used in symmetrical gaits. This presumably unique feature of primate locomotion has been attributed to an ancestral adaptation for cautious arboreal quadrupedalism on thin, flexible branches. However, the functional significance of DS gait remains largely hypothetical. The study presented here tests hypotheses about the functional significance of DS gait by analyzing the gait mechanics of a primate that alternates between DS and lateral sequence (LS) gaits, Cebus apella. Kinematic and kinetic data were gathered from two subjects as they moved across both terrestrial and simulated arboreal substrates. These data were used to test four hypotheses: (1) locomotion on arboreal supports is associated with increased use of DS gait, (2) DS gait is associated with lower peak vertical substrate reaction forces than LS gait, (3) DS gait is associated with greater forelimb/hind limb differentiation in force magnitudes, and (4) DS gait offers increased stability. Our results indicate that animals preferred DS gait on the arboreal substrate, and LS gait while on the ground. Peak vertical substrate reaction forces showed a tendency to be lower in DS gait, but not consistently so. Pole ("arboreal") forces were lower than ground forces in DS gait, but not in LS gait. The preferred symmetrical gait on both substrates was a grounded run or amble, with the body supported by only one limb throughout most of the stride. During periods of bilateral support, the DS gait had predominantly diagonal support couplets. This benefit for stability on an arboreal substrate is potentially outweighed by overstriding, its associated ipsilateral limb interference in DS gait and hind foot positioning in front of the hand on untested territory. DS gait also did not result in an optimal anchoring position of the hind foot under the center of mass of the body at forelimb touchdown. In sum, the results are mixed regarding the superiority of DS gait in an arboreal setting. Consequently, the notion that DS gait is an ancestral adaptation of primates, conditioned by the selection demands of an arboreal environment, remains largely hypothetical.     

行走模式对人体下肢三维步态、肌电信号的影响

目的:揭示人体在主动和被动两种行走模式下的步态特征与下肢主要肌群的肌电信号变化规律。方法:选取12名在校男大学生,通过Greenjog履带式自发力跑台和h/p/cosmos电动跑台建立主动式和被动式行走模型,先后在两种模式下以3种递增速度即慢速(2 km/h)、常速(4 km/h)、和快速(6 km/h)进行一次性步行运动,运用三维运动捕捉分析系统和表面肌电测试仪,分别对每种速度采集2 min的连续三维步态和肌电信号数据。结果:慢速时,被动式行走的支撑相占比显著高于主动式行走(P<0.05),而摆动相占比和膝关节角度变化值则显著低于主动式行走(P<0.05);常速时,被动式行走的膝关节角度变化值和股二头肌积分肌电值显著低于主动式行走(P<0.05);快速时,被动式行走的膝关节、踝关节角度变化值和股二头肌积分肌电值显著低于主动式行走(P<0.01);此外,随着步行速度的增加,被动式行走的胫骨前肌积分肌电值呈现显著增高的趋势(P<0.05)。结论:随着步行速度的增加,人体主动步行时的膝关节活动范围更充分,对主动肌的锻炼作用更明显。     

Footfall patterns and interlimb co-ordination in opossums (Family Didelphidae): evidence for the evolution of diagonal-sequence walking gaits in primates

Most primates typically use a diagonal-sequence footfall pattern during walking. This footfall pattern, which is unusual for mammals, is believed to have originated in ancestral primates in association with the use of grasping extremities for movement and foraging on thin, flexible branches. This theory was tested by comparing gait parameters between the grey short-tailed opossum Monodelphis domestica and the woolly opossum Caluromys philander , two didelphid marsupials that are strongly differentiated in grasping morphology of the extremities and in their reliance on foraging strategies involving thin branches. One hundred and thirty gait cycles were analysed quantitatively from videotapes of subjects moving quadrupedally on a runway and on poles of different diameters (7 and 28 mm). Duty factor (i.e. duration of the stance phase as a percentage of the stride period) for the forelimb and hindlimb, as well as diagonality (i.e. phase relationship between the forelimb and hindlimb cycles), were calculated for each of these symmetrical gait cycles. We found that the highly terrestrial Monodelphis , like most other non-primate mammals, relies primarily on lateral-sequence walking gaits on both runway and poles, and has relatively higher forelimb duty factors. Like primates, the highly arboreal Caluromys uses primarily diagonal-sequence walking gaits on the runway and pole, with relatively higher hindlimb duty factors and diagonality. The fact that the woolly opossum, a marsupial with primate-like feet that moves and forages mainly on thin branches, uses primarily diagonal-sequence gaits when walking supports the view that primate gaits evolved to meet the demands of locomotion on narrow supports. This also demonstrates the functional role of a grasping foot, in association with relatively higher hindlimb duty factors, protraction, and substrate reaction forces, in the production of such walking gaits.     

Functional morphology of the hallucal metatarsal with implications for inferring grasping ability in extinct primates

Primate evolutionary morphologists have argued that selection for life in a fine branch niche resulted in grasping specializations that are reflected in the hallucal metatarsal (Mt1) morphology of extant “prosimians”, while a transition to use of relatively larger, horizontal substrates explains the apparent loss of such characters in anthropoids. Accordingly, these morphological characters—Mt1 torsion, peroneal process length and thickness, and physiological abduction angle—have been used to reconstruct grasping ability and locomotor mode in the earliest fossil primates. Although these characters are prominently featured in debates on the origin and subsequent radiation of Primates, questions remain about their functional significance. This study examines the relationship between these morphological characters of the Mt1 and a novel metric of pedal grasping ability for a large number of extant taxa in a phylogenetic framework. Results indicate greater Mt1 torsion in taxa that engage in hallucal grasping and in those that utilize relatively small substrates more frequently. This study provides evidence that Carpolestes simpsoni has a torsion value more similar to grasping primates than to any scandentian. The results also show that taxa that habitually grasp vertical substrates are distinguished from other taxa in having relatively longer peroneal processes. Furthermore, a longer peroneal process is also correlated with calcaneal elongation, a metric previously found to reflect leaping proclivity. A more refined understanding of the functional associations between Mt1 morphology and behavior in extant primates enhances the potential for using these morphological characters to comprehend primate (locomotor) evolution. Am J Phys Anthropol 156:327–348, 2015. © 2014 Wiley Periodicals, Inc.     

Effects of proximity and behavioral context on acoustic variation in the coo calls of Japanese macaques

Acoustic features of coo calls in Japanese macaques (Macaca fuscata) show large and graded variation. To explore the relevance of acoustic variation in coo calls, I examined whether acoustic features differed by the caller's activity and proximity to group members. The subjects were five adult females from a wild, habituated group of Japanese macaques consisting of 23 individuals. Coo calls from the five females were recorded with their activity and proximity to group members. Acoustic features of 280 calls were measured with a sound spectrograph. Some of the acoustic variables differed by proximity but not by activity. The callers produced coo calls with larger frequency modulation and longer duration when they were far from group members compared to when they were near another member. The results suggest that Japanese macaques produce calls with more detectable and locatable features depending on the proximity to group members.     

Effects of proximity and activity on visual and auditory monitoring in wild Japanese macaques

Group-living primates monitor group members to maintain the spatial cohesiveness of the group. We examined the possibility that visual scanning (turning the head for more than 3 sec) and contact calls (coo calls) function as visual and auditory monitoring behaviors to avoid separation from group members in wild Japanese macaques. The rate of visual scanning increased as proximity to group members decreased and as mobile activities (foraging and moving) increased, compared with immobile activities (resting and grooming). However, the rate of contact calls varied differently with proximity and activities. During resting and moving, the rate of contact calls increased as proximity decreased. In contrast, the rate increased with closer proximity during feeding. Visual scanning during all activities and contact calls during resting and moving increased when the group members were likely to spread over a larger area, suggesting that these behaviors functioned as monitoring of group members to avoid separation from the group. Contact calls also increased when the group members stayed in close proximity during foraging, suggesting that this behavior was also associated with competitive situations. Contact calls may also function to ease tension or maintain distance to avoid conflict in competitive situations.     

Effects of support size and orientation on symmetric gaits in free-ranging tamarins of Amazonian Peru: implications for the functional significance of primate gait sequence patterns

The adoption of a specific gait sequence pattern during symmetrical locomotion has been proposed to have been a key advantage for the exploitation of the fine branch niche in early primates. Diverse aspects of primate locomotion have been extensively studied in technically equipped laboratory settings, but evolutionary conclusions derived from these investigations have rarely been verified in wild primates. Bridging the gap from the lab to the field, we conducted an actual performance determination of symmetrical gaits in two free-ranging tamarin species (Saguinus mystax and Saguinus fuscicollis) of Amazonian Peru by analyzing high-speed video recordings of naturally occurring locomotor bouts. Tamarins arguably represent viable models for aspects of early primate locomotion. We tested three specific hypotheses derived from laboratory studies to test for the influence of support size and orientation and to gain further insight into the functional significance of primate gait sequence patterns: (1) The tamarins utilize symmetrical gaits at a higher rate on small supports than on larger ones. (2) During symmetrical locomotion on small supports, diagonal sequences are utilized at a higher rate than on larger supports. (3) On inclines, diagonal sequences are predominantly used and on declines, lateral sequences are predominantly used. Our results corroborated hypotheses 1 and 3. We found no clear support for hypothesis 2. In conclusion, our results add to the notion that primate gait plasticity, rather than uniform adoption of diagonal sequence gaits, enabled early primates to accommodate different support types and effectively exploit the small branch niche.     

A resampling approach and implications for estimating the phalangeal index from unassociated hand bones in fossil primates

Primate fossil assemblages often have metacarpals and phalanges from which functional/behavioral interpretations may be inferred. For example, intrinsic hand proportions can indicate hand function and substrate use. But, estimates of intrinsic hand proportions from unassociated hand elements can be imperfect due to digit misattribution. Although isolated metacarpals can be identified to a specific digit, phalanges are difficult to assign to a specific ray. We used a resampling approach to evaluate how estimates of intrinsic hand proportions are affected by such uncertainty. First, the phalangeal index—intermediate phalanx length plus proximal phalanx length divided by metacarpal length—for the third digit was calculated for associated specimens of terrestrial, semiterrestrial, and arboreal taxa. We then used resampling procedures to generate distributions of “composite digits” based on resampled ratios in which phalanges from the second, fourth, and fifth rays, and from different individuals, were chosen randomly. Results confirm that the phalangeal index for associated third digits significantly discriminates groups. We also found that resampled ratios had significantly lower means, indicating that using composite digits is prone to systematic underestimation. Resampled ratios also generated distributions with greater variance around the means that obscured distinctions between groups, although significant differences between the most arboreal and terrestrial taxa are maintained. We conclude that using unassociated phalanges to calculate a phalangeal index is prone to sampling bias. Nevertheless, a resampling approach has the potential to inform estimates of hand proportions for fossil taxa, provided that the comparative sample is constrained to mimic the fossil composition. Am J Phys Anthropol 151:280–289, 2013. © 2013 Wiley Periodicals, Inc.     

A biomechanical approach on the optimal stance of Anhanguera piscator (Pterodactyloidea) and its implications for pterosaur gait on land

The stance of pterosaurs on land is traditionally a controversial question. Here, we show that pterosaurs like Anhanguera piscator were quadrupeds. An osteological model of A. piscator was three-dimensionally built in digital space. The reconstructed muscles of its pelvic girdle were then placed on their points of origin and insertion to allow the biomechanical calculations to find the most efficient stance on land to be performed. The hindlimb readjustment (i.e. the repositioning of the hindlimb according to the achieved results) led to a pelvic counterclockwise displacement at 10°, which means that the ilium previously placed at 0° regarding an axis parallel to the ground was moved (and so the whole pelvis) 10° up from the preacetabular process. This new position prevents A. piscator from having a fully upright stance. A 10° displacement of the pelvic girdle would compel the forelimbs to be highly sprawled. Therefore, this study affords A. piscator having a quadrupedal gait and demonstrates that a bipedal stance is not viable once the lever arm values decrease abruptly both for extensor and flexor muscles during the femoral extension. This is the first time this approach is used to shed light on this question.     

Lateral sequence walking in infant Papio cynocephalus: implications for the evolution of diagonal sequence walking in primates

One of the most distinctive aspects of primate quadrupedal walking is the use of diagonal sequence footfalls in combination with diagonal-couplets interlimb timing. Numerous hypotheses have been offered to explain why primates might have evolved this type of gait, yet this important question remains unresolved. Because infant primates use a wider variety of quadrupedal gaits than do adults, they provide a natural experiment with which to test hypotheses about the evolution of unique aspects of primate quadrupedalism. In this study, we present kinematic data on two infant baboons (Papio cynocephalus) in order to test the recent hypothesis that diagonal sequence, diagonal couplets walking might have evolved in primates because their limb positioning provides stability in a small branch environment (Cartmill et al. [2002] Zool J Linn Soc 136:401-420). To assess hindlimb position at the moment of forelimb touchdown, we measured hindlimb angular excursion and ankle position for 84 walking strides, across three different types of gaits (diagonal sequence, diagonal couplets (DSDC); lateral sequence lateral couplets (LSLC); and lateral sequence diagonal couplets (LSDC)). Results indicate that if a forelimb were to contact an unstable substrate, LSLC walking provides as much, and perhaps more, stability when compared to DSDC walking. Therefore, it appears that this moment in a stride was unlikely to be a particularly important selective factor in the evolution of DSDC walking. Further insight into this issue will likely be gained by observations of primate quadrupedalism in natural environments, where the use of lateral sequence gaits might be more common than currently known.     

Limb posture and gait in Numidotherium koholense, a primitive proboscidean from the Eocene of Algeria

The tapir-sized late Early Eocene proboscidean, Numidotherium koholense , is the oldest known member of the mammalian order to which the living elephants belong. Morphology of the limb skeleton is reviewed and newly discovered elements are described, with emphasis placed on features considered to have a bearing on limb posture and locomotion. Structure of the shoulder joint and the fact that the antebrachium is fused in a supinated position, indicates that forelimb posture would have been of the abducted or semi-sprawling type. The carpus, while exhibiting the typically proboscidean serial arrangement of carpals (no contact between unciform and lunar), also possesses a free os centrale. The presence of an os centrale and entepicondylar foramen in the humerus are unexpected eutherian plesiomorphies. The structure of the hip joint indicates an abducted hindlimb posture. In both the fore- and hindlimb, mechanisms exist at the major joints to cope with the complicated flexion-extension paths typical of a semi-sprawling gait. Both the carpus and tarsus are indicative of a plantigrade stance. This, in concert with an abducted limb posture, indicates that the gait in numidotheres contrasts markedly with the sub-unguligrade, parasagittal gait of elephantiform proboscideans. The recent suggestion that Proboscidea have their origins in a cursorially adapted phenacodontid-like stock receives no support from this analysis.     

A new case of fish-eating in Japanese macaques: implications for social constraints on the diffusion of feeding innovation

This is the first detailed report of social factors affecting fish-eating in Japanese macaques under natural circumstances. We video-recorded a complete event of fish eating, involving a new fish food species for the monkeys on Koshima island. Following the discovery of a large beached sea bass by a peripheral male, we observed a total of 16 individuals feeding on the fish in turns, and interacting around it. The rank order of access to the fish was mainly explained by the spatial position of group members, whereas dominance determined how long the fish was monopolized. Although limited, the tolerated presence of close-bystanders while feeding was affected by kinship and affiliation. Genealogic data suggested that fish-eating behavior was well maintained in terms of maternal lineages. This report should contribute to a better understanding of how social features may constrain the long-term diffusion of feeding innovations in free-ranging primate groups.     

Additional postcranial remains of omomyid primates from the Uinta Formation, Utah and implications for the locomotor behavior of large-bodied omomyids

Most omomyids are relatively small bodied (e.g. <500 g), but beginning in the middle Eocene, some omomyids began to grow larger. The largest omomyids occur in the late middle Eocene during the Uintan NALMA, reaching an estimated body mass over 1 kg. The hind limb skeleton of small omomyids is relatively well known, and is generally thought to show active arboreal quadrupedal and leaping adaptations. New postcranial specimens of previously unknown elements from the larger Uintan omomyids, Ourayia (two species), Chipetaia lamporea, and Mytonius hopsoni have recently been recovered from the Uinta Formation, Utah, and from the Mission Valley Formation, California, and they provide additional information concerning their locomotor behavior.The new specimens include several distal tibiae, partial calcanei, a complete talus and a proximal first metatarsal of Chipetaia; distal femora, distal tibiae, cuboids, and partial calcanei of Ourayia uintensis; a complete calcaneus of Ourayia sp.; and a partial calcaneus and talus of Mytonius. Metric analysis of these elements, together with qualitative observations of non-metric traits, indicate that Ourayia and Chipetaia show equal or greater development of traits associated with leaping behavior (including elongation of the calcaneus, navicular and cuboid) than do smaller omomyids from North America. The elements of Mytonius, although fragmentary, lack some leaping features that are well-developed in Ourayia and Chipetaia, suggesting that Mytonius may have relied more on arboreal quadrupedal locomotion than on leaping.     

Development of the supralaryngeal vocal tract in Japanese macaques: implications for the evolution of the descent of the larynx

The configuration of the supralaryngeal vocal tract depends on the nonuniform growth of the oral and pharyngeal portion. The human pharynx develops to form a unique configuration, with the epiglottis losing contact with the velum. This configuration develops from the great descent of the larynx relative to the palate, which is accomplished through both the descent of the laryngeal skeleton relative to the hyoid and the descent of the hyoid relative to the palate. Chimpanzees show both processes of laryngeal descent, as in humans, but the evolutionary path before the divergence of the human and chimpanzee lineages is unclear. The development of laryngeal descent in six living Japanese macaque monkeys, Macaca fuscata, was examined monthly during the first three years of life using magnetic resonance imaging, to delineate the present or absence of these two processes and their contributions to the development of the pharyngeal topology. The macaque shows descent of the hyoid relative to the palate, but lacks the descent of the laryngeal skeleton relative to the hyoid and that of the EG from the VL. We argue that the former descent is simply a morphological consequence of mandibular growth and that the latter pair of descents arose in a common ancestor of extant hominoids. Thus, the evolutionary path of the great descent of the larynx is likely to be explained by a model comprising multiple and mosaic evolutionary pathways, wherein these developmental phenomena may have contributed secondarily to the faculty of speech in the human lineage.