Primate Locomotor Evolution Research Articles

The northern treeshrew (Scandentia: Tupaiidae: Tupaia belangeri) in the context of primate locomotor evolution: A comprehensive analysis of gait, positional, and grasping behavior.

The locomotor behaviors of treeshrews are often reported as scurrying "squirrel-like" movements. As such, treeshrews have received little attention beyond passing remarks in regard to primate locomotor evolution. However, scandentians vary considerably in habitat and substrate use, thus categorizing all treeshrew locomotion based on data collected from a single species is inappropriate. This study presents data on gait characteristics, positional, and grasping behavior of the northern treeshrew (Tupaia belangeri) and compares these findings to the fat-tailed dwarf lemur (Cheirogaleus medius) to assess the role of treeshrews as a model for understanding the origins of primate locomotor and grasping evolution. We found that northern treeshrews were primarily arboreal and shared their activities between quadrupedalism, climbing and leaping in rates similar to fat-tailed dwarf lemurs. During quadrupedal locomotion, they exhibited a mixture of gait characteristics consistent with primates and other small-bodied non-primate mammals and demonstrated a hallucal grasping mode consistent with primates. These data reveal that northern treeshrews show a mosaic of primitive mammalian locomotor characteristics paired with derived primate features. Further, this study raises the possibility that many of the locomotor and grasping characteristics considered to be "uniquely" primate may ultimately be features consistent with Euarchonta.

Asymmetrical gait kinematics of free-ranging callitrichine primates in response to changes in substrate diameter and orientation.

Arboreal environments present considerable biomechanical challenges for animals moving and foraging among substrates varying in diameter, orientation and compliance. Most studies of quadrupedal gait kinematics in primates and other arboreal mammals have focused on symmetrical walking gaits and the significance of diagonal sequence gaits. Considerably less research has examined asymmetrical gaits, despite their prevalence in small-bodied arboreal taxa. Here, we examined whether and how free-ranging callitrichine primates adjust asymmetrical gait kinematics to changes in substrate diameter and orientation, as well as how variation in gait kinematics affects substrate displacement. We used high-speed video to film free-ranging Saguinus tripartitus and Cebuella pygmaea inhabiting the Tiputini Biodiversity Station, Ecuador. We found that S. tripartitus used bounding and half-bounding gaits on larger substrates versus gallops and symmetrical gaits on smaller substrates, and also shifted several kinematic parameters consistent with attenuating forces transferred from the animal to the substrate. Similarly, C. pygmaea shifted from high-impact bounding gaits on larger substrates to using more half-bounding gaits on smaller substrates; however, kinematic adjustments to substrate diameter were not as profound as in S. tripartitus Both species adjusted gait kinematics to changes in substrate orientation; however, gait kinematics did not significantly affect empirical measures of substrate displacement in either species. Because of their small body size, claw-like nails and reduced grasping capabilities, callitrichines arguably represent extant biomechanical analogs for an early stage in primate evolution. As such, greater attention should be placed on understanding asymmetrical gait dynamics for insight into hypotheses concerning early primate locomotor evolution. .

The mechanical origins of arm-swinging

Arm-swinging is a locomotor mode observed only in primates, in which the hindlimbs no longer have a weight bearing function and the forelimbs must propel the body forward and support the entirety of the animal's mass. It has been suggested that the evolution of arm-swinging was preceded by a shift to inverted quadrupedal walking for purposes of feeding and balance, yet little is known about the mechanics of limb use during inverted quadrupedal walking. In this study, we test whether the mechanics of inverted quadrupedal walking make sense as precursors to arm-swinging and whether there are fundamental differences in inverted quadrupedal walking in primates compared to non-primate mammals that would explain the evolution of arm-swinging in primates only. Based on kinetic limb-loading data collected during inverted quadrupedal walking in primates (seven species) and non-primate mammals (three species), we observe that in primates the forelimb serves as the primary propulsive and weight bearing limb. Additionally, heavier individuals tend to support a greater distribution of body weight on their forelimbs than lighter ones. These kinetic patterns are not observed in non-primate mammals. Based on these findings, we propose that the ability to adopt arm-swinging is fairly simple for relatively large-bodied primates and merely requires the animal to release its grasping foot from the substrate. This study fills an important gap concerning the origins of arm-swinging and illuminates previously unknown patterns of primate locomotor evolution.

Behavioral implications of ontogenetic changes in intrinsic hand and foot proportions in olive baboons (Papio Anubis).

Relatively long digits are considered to enhance grasping performance in primates. We tested whether growth-related changes in intrinsic hand and foot proportions may have behavioral implications for growing animals, by examining whether ontogenetic changes in digital proportions are related to variation in voluntary grasping behaviors in baboons. Longitudinal morphological and behavioral data were collected on 6 captive olive baboons (Papio anubis) as they aged from 5 to 22 months. The length of digits and metapodials, measured from radiographs, were used to calculate phalangeal indices (i.e., PIs: summed length of non-distal phalanges relative to corresponding metapodial length). We also examined the allometric scaling of digital bones relative to body mass. We observed baboon positional behaviors over a 15-day period following the radiographic sessions, quantifying the frequency of forelimb and hindlimb grasping behaviors. PIs for all digits declined during growth, a result of the differential scaling of metapodials (which scaled to body mass with isometry) versus phalanges (which scaled with negative allometry). The incidence of forelimb and hindlimb grasping behaviors declined with age. Though we found no relationship between forelimb grasping and hand proportions, the incidence of hindlimb grasping was directly correlated with postaxial digit PIs. Only changes in the intrinsic proportions of the pedal digits are associated with variation in grasping activity in growing baboons. This finding accords previous biomechanical and neuroanatomical studies showing distinct functional roles for the hands and feet during primate locomotion, and has important implications for reconstructing primate locomotor evolution.

Effects of Substrate Size and Orientation on Quadrupedal Gait Kinematics in Mouse Lemurs (Microcebus murinus).

As the smallest living primate, the mouse lemur is a suitable model for reconstructing the locomotor mechanisms by which primate ancestors might have responded to the challenges of an arboreal environment. In this study, we tested the effects of substrate diameter and orientation on quadrupedal gait kinematics in mouse lemurs (Microcebus murinus). Mouse lemurs highly preferred asymmetrical to symmetrical gaits as they moved across a flat board and poles of three diameters (2.5, 1.0, and 0.5cm), set at horizontal, 30° inclined, and 30° declined orientations. During symmetrical gaits, mouse lemurs used diagonal sequence walking and ambling gaits on the same substrates and at the same duty factors for which some similarly sized nonprimate mammals use lateral sequence gaits, suggesting that reliance on diagonal sequence walking in primates may not be explicitly a response to body size relative to substrate diameter. When using asymmetrical gaits, kinematic adjustments to small diameter and/or nonhorizontal substrates included a preference for transverse gallops over other gaits, the avoidance of whole-body suspensions, increases in limb contact duration, and increases in the time interval between the landing of trailing and leading limbs. All of these adjustments are consistent with increasing locomotor stability by dampening center of mass movements and reducing the forces imparted to the substrate. Like mouse lemurs, small-bodied ancestral primates likely used symmetrical gaits occasionally, but more frequently used asymmetrical gaits that were adjusted in response to challenging substrates. Therefore, asymmetrical gait dynamics should be incorporated into hypotheses addressing early primate locomotor evolution.

Single-limb force data for two lemur species while vertically clinging.

Vertical clinging and climbing have been integral to hypotheses about primate origins, yet little is known about how an animal with nails instead of claws resists gravity while on large, vertical, and cylindrical substrates. Here we test models of how force is applied to maintain posture, predicting (1) the shear component force (Fs ) at the hands will be higher than the feet; (2) the normal component force (Fn ) at the feet will be relatively high compared to the hands; (3) the component force resisting gravity (Fg ) at the feet will be relatively high compared to the hands; (4) species with a high frequency of vertical clinging postures will have low Fg at the hands due to relatively short forelimbs. Using a novel instrumented support, single-limb force data were collected during clinging postures for the hands and feet and compared across limbs and species for Propithecus verreauxi (N = 2), a habitual vertical clinger and leaper, and Varecia variegata (N = 3), a habitual above-branch arboreal quadruped. For both species, hand Fs were significantly higher than at the feet and Fn and Fg at the feet were significantly higher than at the hands. Between species, P. verreauxi has relatively low Fg at the hands and Fn at the feet than V. vareigata. These results support previous models and show that hindlimb loading dominance, characteristic of primate locomotion, is found during clinging behaviors and may allow the forelimbs to be used for foraging while clinging. These findings provide insight into selective pressures on force distribution in primates and primate locomotor evolution.

Angular momentum and arboreal stability in common marmosets (Callithrix jacchus).

Despite the importance that concepts of arboreal stability have in theories of primate locomotor evolution, we currently lack measures of balance performance during primate locomotion. We provide the first quantitative data on locomotor stability in an arboreal primate, the common marmoset (Callithrix jacchus), predicting that primates should maximize arboreal stability by minimizing side-to-side angular momentum about the support (i.e., Lsup ). If net Lsup becomes excessive, the animal will be unable to arrest its angular movement and will fall. Using a novel, highly integrative experimental procedure we directly measured whole-body Lsup in two adult marmosets moving along narrow (2.5 cm diameter) and broad (5 cm diameter) poles. Marmosets showed a strong preference for asymmetrical gaits (e.g., gallops and bounds) over symmetrical gaits (e.g., walks and runs), with asymmetrical gaits representing >90% of all strides. Movement on the narrow support was associated with an increase in more "grounded" gaits (i.e., lacking an aerial phase) and a more even distribution of torque production between the fore- and hind limbs. These adjustments in gait dynamics significantly reduced net Lsup on the narrow support relative to the broad support. Despite their lack of a well-developed grasping apparatus, marmosets proved adept at producing muscular "grasping" torques about the support, particularly with the hind limbs. We contend that asymmetrical gaits permit small-bodied arboreal mammals, including primates, to expand "effective grasp" by gripping the substrate between left and right limbs of a girdle. This model of arboreal stability may hold important implications for understanding primate locomotor evolution.

Body size and the small branch niche: Using marsupial ontogeny to model primate locomotor evolution

Recently proposed ancestral locomotor and morphological ‘stages’ leading to the evolution of primates have emphasized small body size, and a transition from a clawed non-grasping stage, to a clawed, grasping stage with clawless opposable hallux, to a fully-nailed primate with grasping extremities. This evolutionary transition was presumably associated with frequent use of the small branch niche. To model elements of these evolutionary transitions, we investigate how body size, substrate size, substrate orientation and grasping morphology interact to influence quadrupedal kinematics within and between ontogenetic samples of two small-bodied marsupials, one arboreal (Petaurus breviceps) and the other mainly terrestrial (Monodelphis domestica). Longitudinal morphometric and kinematic data were collected from four juvenile P. breviceps (33–75 g) and two juvenile M. domestica (18–95 g) walking across poles of three diameters (2.5, 1.0, and 0.5 cm) and three orientations (horizontal, 30° incline, 30° decline). The two species responded similarly to some substrate conditions, but diverged in response to others. Kinematic divergence between the two species reflects Monodelphis' relatively shorter digits, reduced grasping ability and greater need for stabilizing mechanisms on narrow substrates. At a given relative body size or pole orientation, Monodelphis used higher limb duty factors, more limbs in support per stride, lower limb phases, and in some conditions, faster speeds compared with Petaurus. Interspecific differences were the least distinct on declined poles, highlighting the particular challenge of this substrate condition, even for arboreally adapted species. Small-bodied, arboreal primate ancestors would likely have employed the kinematic mechanisms common to our model taxa, but those with enhanced grasping adaptations would most likely not have required the increased level of stabilizing mechanisms exhibited by Monodelphis. Thus, using these two species as locomotor models has underscored the functional importance of grasping extremities in primate origins, even if ancestral primates were very small in body size.

The mechanics of acceleration and deceleration in primate quadrupeds:implications for primate locomotor evolution.

The ability to accelerate and decelerate is critical for animal survival and may be a selective priority determining body form in mammals. Studies of quadrupedal mammals have shown that pitching moments around an animal's center of mass (COM) limit maximum acceleration and deceleration and that the ability to resist such moments is influenced by limb length, COM position, and the ability to shift weight to the fore‐ or hindquarters. Primates have relatively long, gracile forelimbs and have higher vertical ground reaction forces on their hindlimbs than forelimbs, unlike most mammals. Primates should then differ from other mammals in that they will be effective in producing acceleration but limited in producing deceleration. This hypothesis was tested with lateral video and single limb forces recorded during accelerating and decelerating steps for two strepsirhine primate species: Eulemur fulvus and Lemur catta. Results show that primates are limited in maximum acceleration and deceleration by their limb length and that they adopt specific mechanical solutions including loading the trailing limb relatively more, initiating decelerations with the hindlimbs rather than the forelimbs, and increasing contact time to limit instantaneous vertical force increases. These solutions are consistent with other unusual primate gait characters associated with adaptations to arboreal locomotion.

The gaits of primates: center of mass mechanics in walking, cantering and galloping ring-tailed lemurs,Lemur catta

Most primates, including lemurs, have a broad range of locomotor capabilities, yet much of the time, they walk at slow speeds and amble, canter or gallop at intermediate and fast speeds. Although numerous studies have investigated limb function during primate quadrupedalism, how the center of mass (COM) moves is not well understood. Here, we examined COM energy, work and power during walking, cantering and galloping in ring-tailed lemurs, Lemur catta (N=5), over a broad speed range (0.43-2.91 m s(-1)). COM energy recoveries were substantial during walking (35-71%) but lower during canters and gallops (10-51%). COM work, power and collisional losses increased with speed. The positive COM works were 0.625 J kg(-1) m(-1) for walks and 1.661 J kg(-1) m(-1) for canters and gallops, which are in the middle range of published values for terrestrial animals. Although some discontinuities in COM mechanics were evident between walking and cantering, there was no apparent analog to the trot-gallop transition across the intermediate and fast speed range (dimensionless v>0.75, Fr>0.5). A phenomenological model of a lemur cantering and trotting at the same speed shows that canters ensure continuous contact of the body with the substrate while reducing peak vertical COM forces, COM stiffness and COM collisions. We suggest that cantering, rather than trotting, at intermediate speeds may be tied to the arboreal origins of the Order Primates. These data allow us to better understand the mechanics of primate gaits and shed new light on primate locomotor evolution.

Comparative triceps surae morphology in primates: a review.

Primate locomotor evolution, particularly the evolution of bipedalism, is often examined through morphological studies. Many of these studies have examined the uniqueness of the primate forelimb, and others have examined the primate hip and thigh. Few data exist, however, regarding the myology and function of the leg muscles, even though the ankle plantar flexors are highly important during human bipedalism. In this paper, we draw together data on the fiber type and muscle mass variation in the ankle plantar flexors of primates and make comparisons to other mammals. The data suggest that great apes, atelines, and lorisines exhibit similarity in the mass distribution of the triceps surae. We conclude that variation in triceps surae may be related to the shared locomotor mode exhibited by these groups and that triceps surae morphology, which approaches that of humans, may be related to frequent use of semiplantigrade locomotion and vertical climbing.

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.

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.

Adaptive value of ambling gaits in primates and other mammals

At speeds between the walk and the gallop, most mammals trot. Primates almost never trot, and it has been claimed that they transition directly from a walk to a gallop without any distinctive mid-speed running gait. If true, this would be another characteristic difference between the locomotion of primates and that of most other quadrupedal mammals. Presently, however, few data exist concerning the actual presence or absence of intermediate-speed gaits (i.e. gaits that are used between a walk and a gallop) in primates. Video records of running in twelve primate species reveal that, unlike most other mammals, all the primates studied almost exclusively adopt an 'amble'--an intermediate-speed running gait with no whole-body aerial phase--rather than trot. Ambling is also common in elephants and some horses, raising the question of why ambling is preferred over trotting in these diverse groups of animals. Mathematical analyses presented here show that ambling ensures continuous contact of the body with the substrate while dramatically reducing vertical oscillations of the center of mass. This may explain why ambling appears to be preferable to trotting for extremely large terrestrial mammals such as elephants and for arboreal mammals like primates that move on unstable branches. These findings allow us to better understand the mechanics of these unusual running gaits and shed new light on primate locomotor evolution.

Substrate alters forelimb to hindlimb peak force ratios in primates

It is often claimed that the walking gaits of primates are unusual because, unlike most other mammals, primates appear to have higher vertical peak ground reaction forces on their hindlimbs than on their forelimbs. Many researchers have argued that this pattern of ground reaction force distribution is part of a general adaptation to arboreal locomotion. This argument is frequently used to support models of primate locomotor evolution. Unfortunately, little is known about the force distribution patterns of primates walking on arboreal supports, nor do we completely understand the mechanisms that regulate weight distribution in primates. We collected vertical peak force data for seven species of primates walking quadrupedally on instrumented terrestrial and arboreal supports. Our results show that, when walking on arboreal vs. terrestrial substrates, primates generally have lower vertical peak forces on both limbs but the difference is most extreme for the forelimb. We found that force reduction occurs primarily by decreasing forelimb and, to a lesser extent, hindlimb stiffness. As a result, on arboreal supports, primates experience significantly greater functional differentiation of the forelimb and hindlimb than on the ground. These data support long-standing theories that arboreal locomotion was a critical factor in the differentiation of the forelimbs and hindlimbs in primates. This change in functional role of the forelimb may have played a critical role in the origin of primates and facilitated the evolution of more specialized locomotor behaviors.

Forelimb mechanics as a function of substrate type during quadrupedalism in two anthropoid primates

During the past century, many anthropologists have proposed that hominoid orthograde locomotion arose in an arboreal quadrupedal ancestor with highly mobile, low weight-bearing forelimbs. However, no quantitative data comparing kinematic and kinetic aspects of forelimb use during arboreal and terrestrial quadrupedalism have been available to evaluate such theories. In this preliminary study, a spider monkey and a baboon were videotaped in three planes while walking quadrupedally on an instrumented runway and a raised instrumented horizontal pole. Forelimb angles and substrate reaction force resultants were calculated for each animal on each substrate. The quantitative data presented here support previous models for the evolution of primate locomotion that were based on theoretical biomechanics and qualitative or anecdotal evidence. In addition, this study has revealed several previously undocumented accommodations to "arboreal" quadrupedal locomotion in these two primates. While walking on the pole, compared to travel on the ground, (1) both animals adopted a "crouched" forelimb posture, but only the spider monkey abducted its arm and ulnar deviated its hand; (2) both subjects have lower resultant forces on the forelimb due to lower absolute force magnitudes and changes in the timing of component peaks; and (3) both animals reduce and reorient transverse forces. Similar accommodations to arboreal travel by both subjects appear to be mechanical requirements of arboreal locomotion. However, differences may be due to morphological differences between the subjects, or to their divergent phylogenetic history. These results are used to explore potential explanations for the morphological differences between arboreal and terrestrial primate quadrupeds in terms of bone and joint strain and to evaluate models of primate locomotor evolution.