Primate Locomotion

Life in the trees requires a constant stream of body adjustments (Figure 1). Primates are fantastic leapers (Figure 2), swift arboreal quadrupeds, arm-swingers, and vertical clingers. In fact, primates possess one of the most varied movement arrays of all mammals. As a group, primates are hind-limb dominated. They utilize a diagonal couplet gait and they tend to bend their elbows and knees (Figure 3) as they move along branches (Hildebrand, 1967; Napier, 1967; Martin, 1972; Kimura et al., 1979; Rollinson & Martin, 1988; Demes et al., 1994; Schmitt, 1995; Larson, 1998, Larson et al., 2001; Cartmill et al., 2002). All of these characteristics help maintain balance along a curved surface. Despite what is written in most introductory textbooks, primate bodies are not generalized but are in fact quite specialized for life in the trees.

Positional behavior is the term primatologists use to describe body postures with movements (see Prost, 1965; Rose, 1973, 1974; Hunt et al. 1996 for a list of postures and movements). Most postures are quite static. For example, sitting (Figure 4), standing, or lying down (Figure 5) are frequently observed among living primate postural patterns. These are often described as resting postures. Postures such as cantilevering, vertical clinging, tail suspension, or foot hanging (Figure 6), which are associated with specific species, are often linked to obtaining food. A few body adaptations, for example prehensile tails, arm-hanging anatomy, and ischial callosities, are associated with a primate posture, but most are not. In contrast, primate locomotion is body-active relative to postures, and thus musculoskeletal anatomy is more often associated with movement adaptations (for example, the long legs of leaping primates).

Body size is a complicated variable across primate locomotor studies (Napier, 1968; Fleagle & Mittermeier, 1980; Gebo & Chapman, 1995; McGraw, 1998; Fleagle, 1999). Size patterns can be taxonomically constrained while comparisons across groups show odd patterns. For example, there are small and large leaping primates as well as small and large brachiators. The same can be said concerning quadrupedalists, whether arboreal or terrestrial. These observations suggest that primatologists have been unable to universally explain how size affects primate locomotion. We can say that 1) larger primates are at greater risk to injury if they fall relative to smaller primates; 2) frequent leaping seems to disappear above 10 kg, and the best primate leapers tend to be small; and 3) climbing is universal across primates, no matter their size.

Body size relative to substrate size or gaps in the canopy does link ecology with primate locomotion. Small primates see more gaps in the canopy than large primates. Small branches are relatively tiny compared to large primates and obviously not capable of supporting heavy weights. In contrast, tree trunks are wide substrates that smaller primates cannot effectively grasp (Cartmill, 1974). Here, body size and the selection of body supports are correlated and species that choose to be exceptions evolve adaptations for these specific habitats (i.e., the claw-like nails of the trunk-clinging callithrichines). In terms of overall tree use, no matter the size of primates, they often divide the top, middle, and lower regions of trees among species to minimize feeding competition with other sympatric primates (Charles-Dominique, 1977).

Grasping is the hallmark adaptation among primate limbs (LeGros Clark, 1959; Cartmill, 1974, 1985; Szalay and Dagosto, 1988; Lewis, 1989). The ability to hold onto small curved surfaces (i.e., tiny branches) has allowed primates to explore the arboreal canopy in great detail. Primates have nails instead of claws, several large intrinsic and extrinsic muscles devoted to digital flexion and grasping, and mobile joint surfaces that allow hand and foot rotations. They also have an opposable first digit as well as wide fingers and toes with broad palms or soles. This greater surface-area contact with arboreal substrates adds stability during arboreal locomotion (Cartmill, 1979). All are key components in grasping.

Palmigrade hands are the active grasping and climbing structures for primates but primate hands reflect a variety of postural types including palmigrade, digitigrade, knuckle-walking, fist-walking, and suspensory hand positions. Fist-walking and knuckle-walking hands allow orangutans and the African apes to fold their long fingers underneath as they move quadrupedally, usually terrestrially (Tuttle, 1967; Susman, 1974). Primates also use their hands to procure and eat their food. Reaching, grasping, and pulling items to the mouth add another dimension to primate hand adaptations (Napier, 1980; Hamrick, 1998, 2001; Schmitt and Lemelin, 2002). This feeding adaptation has figured prominently in the visual predation hypothesis of Cartmill (1972). The secondary evolution of claw-like nails among a variety of different primates (Phaner, a cheirogaleid, Euoticus, a galagid, and callitrichines, New World monkeys) has been tied to both the ecological use of large-diameter trunks — a substrate situation that exceeds the grasping span of hands and feet (Cartmill, 1979) — and to exudate feeding (Charles-Dominique, 1977; Garber, 1992).

Climbing, like grasping, is an ancient arboreal adaptation for primates. Moving up vertical substrates is well documented across all primates, although quantitative studies have shown that climbing is not a particularly frequent movement in any locomotor profile (Gebo, 1996). Leaping, quadrupedalism, or brachiation dominate these profiles. Primates clearly need to climb upward in trees but relative to all other movement types, vertical climbing is not frequent relative to the traveling modes of locomotion. Among climbing primates, apes with their long arms are recorded to be frequent vertical climbers when arboreal, but forelimb lengthening along with their highly modified upper body is likely an adaptation from their arm-swinging ancestry.

Some researchers like to divide climbing into two locomotor categories: vertical climbing and clambering. In this scheme, climbing is restricted to ascending or descending a vertical support whereas clambering is moving obliquely through a network of smaller branches. They differ in the angle of the climb and in the supports on which primates move upward. Clambering is more common among primates than vertical climbing.

Bridging is an unusual movement pattern often associated with climbing movements. Here, a primate stretches across a gap and pulls itself to the branch on the other side. Lorises, atelines, and oranguatans often use this technique to cross gaps in the canopy.

Quadrupedalism can be divided into arboreal (the most common) and terrestrial versions. Quadrupedal primates have fore- and hind limbs of relatively equal length and they tend to lower their centers of gravity toward the branch (Napier, 1967; Larson, 1998) by bending their elbows and knees (Schmitt, 1995). The use of diagonal couplets allows primates to have only a single limb off the substrate at any given time. Arboreal quadrupedal primates supinate their hands and feet toward the curve of the support (palmigrade support). Terrestrial quadrupedal primates have similar fore and hind limb lengths, but these primates (mostly Old World monkeys) have greatly reduced joint mobility throughout their limbs and they utilize more pronated hand positions.

Terrestral quadrupedalism can be subdivided into digitigrade, knuckle-walking, and fist-walking types. The African apes utilize terrestrial quadrupedalism with fingers folded at the first joint (knuckle-walking), and exhibiting longer arms than legs and a back angled at 45 degrees. Orangutans move with a fist-walking hand posture (fingers entirely closed in a fist) and often highly supinated foot positions. Terrestrial Old World monkeys are often digitigrade with their hand positions.

Primates that leap come in two basic varieties. Strepsirhine primates (e.g., lemurs and galagos) and tarsiers are known for their forceful upward parabolic leaps, while anthropoids tend to leap outward along a horizontal plane and then fall downward. Both can leap frequently, although size tends to be limiting. For example, there are few frequent leaping primates above 10 kg. Elongated legs help leapers increase height and distance, producing leaps with less relative muscle force (Hall-Craggs, 1965). All leapers have long femora, but it is the anatomy of the knee, with its tall antero-posterior height and the high lateral patellar rim, that separates the occasional versus the habitual leaper. As one might expect, the muscles of the quadriceps are huge in these animals to produce the necessary leg force for extension to move these primates across canopy gaps quickly and efficiently. Tarsiers have the most extreme hind limbs with tibio-fibular fusion and greatly elongated foot bones. Galagos as well have significantly increased foot length by elongating their foot bones, thereby achieving longer legs and ultimately better lever mechanics. Morton (1924) argued that the reason primates elongated the calcaneus and the navicular bones higher up in the foot instead of their more distal metatarsals is a morphological compromise between the mechanical demands of leaping and grasping. Although long lever arms (i.e., long feet) help produce better gear ratios for greater leaping distances, the feet of arboreal primates must also be able to grasp. By elongating the calcaneus and the navicular, tarsiers and galagos have been able to maintain mobility toward the digits while greatly increasing foot length.

Arm-swinging and arm hanging is a very peculiar primate movement/posture relative to hind limb dominated primates, and it evolved at least twice: in apes and in spider monkeys. The upper body of living apes (including humans) is quite different from those of other primates. All of these upper body features are related to brachiation and arm suspension (Keith, 1923; Washburn, 1968; Gebo, 1996). In apes, the thorax is broad and flattened antero-posteriorly. This is an orthograde or an erect back relative to the common pronograde or horizontal backs of primates. Here, the shoulders are pushed out to the sides of the body with scapulae lying on the back wall rather than along the sides of the rib cage as in quadrupedal primates. This new scapular position forces the shoulder joints to the sides of the body and away from the midline, thereby increasing rotational mobility of the arm. The clavicle is long to reach the new shoulder position. The forelimb is very long overall, thereby increasing stride length (or arm-swing in this case). The lateral position of the shoulder joint constrains the enlarged humeral head joint to twist (medial torsion) to articulate with the lateral facing scapula, thereby allowing the elbow to face forward.

The elbow joint morphology of the living apes allows both large rotational movements and large flexion-extension movements (Rose, 1988). In fact, the olecranon process of the ulna is greatly shortened among apes, allowing for full extension at the elbow joint, an unusual ability relative to other primates, but a necessary condition for a fully extended arm during hanging. The forelimb bones are long among apes, especially in gibbons. At the wrist, apes have increased abduction (Lewis, 1969, 1989), and ape fingers are very long and hook-like relative to other non-swinging primates.