Body mass distribution and gait mechanics in fat-tailed dwarf lemurs (Cheirogaleus medius) and patas monkeys (Erythrocebus patas)

Most quadrupeds walk with lateral sequence (LS) gaits, where hind limb touchdowns are followed by ipsilateral forelimb touchdowns. Primates, however, typically walk with diagonal sequence (DS) gaits, where hind limb touchdowns are followed by contralateral forelimb touchdowns. Because the use of DS gaits is nearly ubiquitous among primates, understanding gait selection in primates is critical to understanding primate locomotor evolution. The Support Polygon Model [Tomita, M., 1967. A study on the movement pattern of four limbs in walking. J. Anthropol. Soc. Nippon 75, 120-146; Rollinson, J., Martin, R.D., 1981. Comparative aspects of primate locomotion, with special reference to arboreal cercopithecines. Symp. Zool. Soc. Lond. 48, 377-427] argues that primates' use of DS gaits stems from a more caudal position of the whole-body center of mass (COM) relative to other mammals. We tested the predictions of the Support Polygon Model by examining the effects of natural and experimental variations in COM position on gait mechanics in two distantly related primates: fat-tailed dwarf lemurs (Cheirogaleus medius) and patas monkeys (Erythrocebus patas). Dwarf lemur experiments compared individuals with and without a greatly enlarged tail (a feature associated with torpor that can be expected to shift the COM caudally). During patas monkey experiments, we experimentally shifted the COM cranially with the use of a weighted belt (7-12% of body mass) positioned above the scapulae. Examination of limb kinematics revealed changes consistent with systematic deviations in COM position. Nevertheless, footfall patterns changed in a direction contrary to the predictions of the Support Polygon Model in the dwarf lemurs and did not change at all in the patas monkey. These results suggest that body mass distribution is unlikely to be the sole determinant of footfall pattern in primates and other mammals.     

The effects of natural substrate discontinuities on the quadrupedal gait kinematics of free‐ranging Saimiri sciureus

Wild primates encounter complex matrices of substrates that differ in size, orientation, height, and compliance, and often move on multiple, discontinuous substrates within a single bout of locomotion. Our current understanding of primate gait is limited by artificial laboratory settings in which primate quadrupedal gait has primarily been studied. This study analyzes wild Saimiri sciureus (common squirrel monkey) gait on discontinuous substrates to capture the realistic effects of the complex arboreal habitat on walking kinematics. We collected high‐speed video footage at Tiputini Biodiversity Station, Ecuador between August and October 2017. Overall, the squirrel monkeys used more asymmetrical walking gaits than symmetrical gaits, and specifically asymmetrical lateral sequence walking gaits when moving across discontinuous substrates. When individuals used symmetrical gaits, they used diagonal sequence gaits more than lateral sequence gaits. In addition, individuals were more likely to change their footfall sequence during strides on discontinuous substrates. Squirrel monkeys increased the time lag between touchdowns both of ipsilaterally paired limbs (pair lag) and of the paired forelimbs (forelimb lag) when walking across discontinuous substrates compared to continuous substrates. Results indicate that gait flexibility and the ability to alter footfall patterns during quadrupedal walking may be critical for primates to safely move in their complex arboreal habitats. Notably, wild squirrel monkey quadrupedalism is diverse and flexible with high proportions of asymmetrical walking. Studying kinematics in the wild is critical for understanding the complexity of primate quadrupedalism.     

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.     

The effect of branch diameter on primate gait sequence pattern

Most mammals use lateral sequence gaits during quadrupedal locomotion, a pattern characterized by the touchdown of a forelimb directly following the ipsilateral hind limb in a given stride cycle. Primates, however, tend to use diagonal sequence (DS) gaits, whereby it is the touchdown of a contralateral forelimb that follows that of a given hind limb most closely in time. A number of scenarios have been offered to explain why primates favor DS gaits, most of them relating to the use of the arboreal habitat and, in particular, the exploitation of a narrow branch niche. This experimental study explores the potential explanation for the use of DS gaits by examining the relationship between branch diameter and gait patterns in 360 strides collected from six species of quadrupedal strepsirrhine primates on broad and narrow diameter supports. Gait sequence is quantified using limb phase, or the percentage of time during a stride cycle that a forelimb touchdown follows an ipsilateral hind limb touchdown. Although Loris, Nycticebus and Eulemur rubriventer individuals in this study did exhibit significantly lower locomotor velocities on narrower supports (P<0.01 in all three species), analyses of covariance showed no significant differences in limb phase values between broad and narrow diameter supports. Hence, results indicate surprisingly little evidence to suggest that alterations in gait sequence pattern provide a specific advantage for negotiating narrow supports.     

Locomotor mechanics of the slender loris (Loris tardigradus)

The quadrupedal walking gaits of most primates can be distinguished from those of most other mammals by the presence of diagonal-sequence (DS) footfall patterns and higher peak vertical forces on the hindlimbs compared to the forelimbs. The walking gait of the woolly opossum (Caluromys philander), a highly arboreal marsupial, is also characterized by diagonal-sequence footfalls and relatively low peak forelimb forces. Among primates, three species--Callithrix, Nycticebus, and Loris--have been reported to frequently use lateral-sequence (LS) gaits and experience relatively higher peak vertical forces on the forelimbs. These patterns among primates and other mammals suggest a strong association between footfall patterns and force distribution on the limbs. However, current data for lorises are limited and the frequency of DS vs. LS walking gaits in Loris is still ambiguous. To test the hypothesis that patterns of footfalls and force distribution on the limbs are functionally linked, kinematic and kinetic data were collected simultaneously for three adult slender lorises (Loris tardigradus) walking on a 1.25 cm horizontal pole. All subjects in this study consistently used diagonal-sequence walking gaits and always had higher peak vertical forces on their forelimbs relative to their hindlimbs. These results call into question the hypothesis that a functional link exists between the presence of diagonal-sequence walking gaits and relatively higher peak vertical forces on the hindlimbs. In addition, this study tested models that explain patterns of force distribution based on limb protraction angle or limb compliance. None of the Loris subjects examined showed kinematic patterns that would support current models proposing that weight distribution can be adjusted by actively shifting weight posteriorly or by changing limb stiffness. These data reveal the complexity of adaptations to arboreal locomotion in primates and indicate that diagonal-sequence walking gaits and relatively low forelimb forces could have evolved independently.     

Stability, limb coordination and substrate type: the ecorelevance of gait sequence pattern in primates

The coordination of limb movements during mammalian locomotion has been well documented in the literature. Most mammals use lateral sequence (LS) gaits, in which a forelimb follows an ipsilateral hind limb during the stride cycle. Primates, however, tend to utilize diagonal sequence (DS) gaits, whereby a contralateral forelimb follows a given hind limb during the stride cycle. A number of scenarios have been offered to explain why primates favor DS gaits, most of them relating to the use of the arboreal habitat and, in particular, the exploitation of a terminal branch niche. Yet to date, there is surprisingly little evidence to support the advantage of DS gaits for negotiating different aspects of the terminal branch environment. Nonetheless, it is apparent that primates possess unique morphologies and a higher than typically recognized degree of flexibility in gait sequence pattern, both of which likely offer advantages for moving upon discontinuous and unstable terminal branches. This paper reviews potential explanations for the use of DS gaits in primates and considers mechanisms by which gait sequence may be altered during different types of arboreal challenges.     

Substrate determines asymmetrical gait dynamics in marmosets (Callithrix jacchus) and squirrel monkeys (Saimiri boliviensis)

Studies of skeletal pathology indicate that injury from falling accounts for most long bone trauma in free‐ranging primates, suggesting that primates should be under strong selection to manifest morphological and behavioral mechanisms that increase stability on arboreal substrates. Although previous studies have identified several kinematic and kinetic features of primate symmetrical gaits that serve to increase arboreal stability, very little work has focused on the dynamics of primate asymmetrical gaits. Nevertheless, asymmetrical gaits typify the rapid locomotion of most primates, particularly in smaller bodied taxa. This study investigated asymmetrical gait dynamics in growing marmosets and squirrel monkeys moving on terrestrial and simulated arboreal supports (i.e., an elevated pole). Results showed that monkeys used several kinematic and kinetic adjustments to increase stability on the pole, including reducing peak vertical forces, limiting center of mass movements, increasing substrate contact durations, and using shorter and more frequent strides (thus limiting disruptive whole‐body aerial phases). Marmosets generally showed greater adjustment to pole locomotion than did squirrel monkeys, perhaps as a result of their reduced grasping abilities and retreat from the fine‐branch niche. Ontogenetic increases in body size had relatively little independent influence on asymmetrical gait dynamics during pole locomotion, despite biomechanical theory suggesting that arboreal instability is exacerbated as body size increases relative to substrate diameter. Overall, this study shows that 1) symmetrical gaits are not the only stable way to travel arboreally and 2) small‐bodied primates utilize specific kinematic and kinetic adjustments to increase stability when using asymmetrical gaits on arboreal substrates. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

Support polygons and symmetricalgaits in mammals

The symmetrical gaits of quadrupedal mammals are oftendescribed in terms of two variables: duty factor (S = the stanceperiod of one foot, as a percentage of the gait cycle) and diagonality(D = the percentage of the cycle period by whichthe left hind footfall precedes the left fore footfall). We showthat support polygons are optimized during walking (i.e.the percentage of the locomotor cycle spent standing on only twofeet is minimized) for: (1) the diagonal-sequence, diagonal-coupletswalks characteristic of primates (50 < D < 75)when D = [hindlimb S]; (2) lateral-sequence,lateral-couplets walks (0 < D < 25)when D = [hindlimb S]− 50;(3) lateral-sequence, diagonal-couplets walks (25 < D < 50)when D = 100 −[forelimb S].To determine whether animal behaviour is optimal in this sense,we examined 346 symmetrical gait cycles in 45 mammal species. Ourempirical data show that mammalian locomotor behaviour approximatesthe theoretical optima. We suggest that diagonal-sequence walkingmay be adopted by ­primates as a means of ensuring thata grasping hindfoot is placed in a protracted position on a testedsupport at the moment when the contralateral forefoot strikes downon an untested support.  © 2002 The Linnean Societyof London, Zoological Journal of the Linnean Society , 2002, 136 ,401−420     

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.     

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. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Squirrel monkey locomotion on an inclined treadmill: Implications for the evolution of gaits

Three adult squirrel monkeys were trained to run on a motor-driven treadmill that was inclined downwardly and upwardly at 8°, 16° and 28°, and horizontally (0°). Films were used to compare the gait and kinematics of the animals across the inclines. All three animals used both lateral and diagonal sequence gaits, although the former was preferred at all but the upward 16° and 28° inclines. Cycle duration and hind limb stance and swing durations tended to increase as downward inclination decreased. Trunk inclination, except at 28° downward, tended to parallel the changes in treadmill inclination. The most dramatic and consistent change for the hind limb joint displacement patterns was that maximum extension during stance increased as the treadmill inclination increased from 28° downward to 28° upward. In contrast to an earlier study by Prost & Sussman (1969), we could find no evidence that squirrel monkeys are best adapted to run on upward inclines of about 16°. The utilization of diagonal sequence gaits on the upward inclines supports previous suggestions that the preference for these gaits in primates is associated with an evolutionary increase in climbing behaviors.     

Three-dimensional kinematics of capuchin monkey bipedalism

Capuchin monkeys are known to use bipedalism when transporting food items and tools. The bipedal gait of two capuchin monkeys in the laboratory was studied with three-dimensional kinematics. Capuchins progress bipedally with a bent-hip, bent-knee gait. The knee collapses into flexion during stance and the hip drops in height. The knee is also highly flexed during swing to allow the foot which is plantarflexed to clear the ground. The forefoot makes first contact at touchdown. Stride frequency is high, and stride length and limb excursion low. Hind limb retraction is limited, presumably to reduce the pitch moment of the forward-leaning trunk. Unlike human bipedalism, the bipedal gait of capuchins is not a vaulting gait, and energy recovery from pendulum-like exchanges is unlikely. It extends into speeds at which humans and other animals run, but without a human-like gait transition. In this respect it resembles avian bipedal gaits. It remains to be tested whether energy is recovered through cyclic elastic storage and release as in bipedal birds at higher speeds. Capuchin bipedalism has many features in common with the facultative bipedalism of other primates which is further evidence for restrictions on a fully upright striding gait in primates that transition to bipedalism. It differs from the facultative bipedalism of other primates in the lack of an extended double-support phase and short aerial phases at higher speeds that make it a run by kinematic definition. This demonstrates that facultative bipedalism of quadrupedal primates need not necessarily be a walking gait.     

Locomotion in degus on terrestrial substrates varying in orientation – implications for biomechanical constraints and gait selection

To gain new insights into running gaits on sloped terrestrial substrates, metric and selected kinematic parameters of the common degu (Octodon degus) were examined. Individuals were filmed at their maximum voluntary running speed using a high-speed camera placed laterally to the terrestrial substrate varying in orientations from −30° to +30°, at 10° increments. Degus used trotting, lateral-sequence (LS) and diagonal-sequence (DS) running gaits at all substrate orientations. Trotting was observed across the whole speed range whereas DS running gaits occurred at significantly higher speeds than LS running gaits. Metric and kinematic changes on sloped substrates in degus paralleled those noted for most other mammals. However, the timing of metric and kinematic locomotor adjustments differed significantly between individual degus. In addition, most of these adjustments took place at 10° rather than 30° inclines and declines, indicating significant biomechanical demands even on slightly sloped terrestrial substrates. The results of this study suggest that DS and LS running gaits may represent an advantage in small to medium-sized mammals for counteracting some level of locomotor instability. Finally, changes in locomotor parameters of the forelimbs rather than the hindlimbs seem to play an important role in gait selection in small to medium-sized mammals.     

Footfall patterns, stride length and speed of vertical climbing in spider monkeys (Ateles fusciceps robustus) and woolly monkeys (Lagothrix lagotricha)

Vertical climbing is central to theories surrounding the locomotor specialisations of large primates. In this paper, we present spatiotemporal gait parameters obtained from video recordings of captive spider monkeys (Ateles fusciceps robustus) and woolly monkeys (Lagothrix lagotricha) in semi-natural enclosures, with the aim of discovering the influence of body weight and differences in general locomotor behaviour on vertical climbing kinematics on various substrates. Results show that there are only few differences between gait parameters of climbing on thin trees, vertical and oblique ropes, while climbing on large-diameter trees differs considerably, reflecting the higher costs of locomotion on the latter. At the same speed, Ateles takes longer strides and the support phase takes a smaller percentage of cycle duration than in Lagothrix. Footfall patterns are more diverse in Ateles and include a higher proportion of ipsilateral limb coupling. Compared to other primates, the gait characteristics of vertical climbing of atelines most closely resemble those of African apes.     

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.     

Symmetrical gaits of primates

Walking and symmetrical running gaits of 26 genera of primates are analyzed using numerical and graphical methods described previously. The raw data are 1701 feet of 16 mm motion picture film mostly exposed at 64 frames per second. Adult monkeys and apes usually use the walking trot or diagonal-sequence walks. Individual monkeys occasionally use lateral-sequence walks resembling those that are usual for human infants. Human children moving on hands and feet use gaits ranging from the walking pace through the lateral-sequence walks to the walking trot. An infant macaque studied from age 17 hours to 96 days first walked with a lateral-sequence, diagonal-couplets gait and then gradually shifted to the diagonal-sequence, diagonal-couplets gait of the adult. Few non-primates use the diagonal-sequence walks which are typical of primates. Typical support sequences are figured. Relative placement of feet and consequent slight asymmetry are described.