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.     

Locomotion and posture in Lagothrix lagotricha

This long-term study of woolly monkey (Lagothrix) locomotor and postural behaviour employs methods identical to those used during a previous study of the locomotion and posture of two species of Ateles, allowing a detailed comparison between the two genera, which are strong competitors in extensive parts of the Amazon basin and northern Andes. As in Ateles, Lagothrix locomotion can be divided into five patterns, based on limb usage: quadrupedal walking and running, suspensory locomotion, climbing, bipedalism (very rare in wild woolly monkeys) and leaping. Lagothrix differs from Ateles primarily in its greater reliance on quadrupedal locomotion during both travel and feeding and on its de-emphasis of the use of suspensory locomotion as compared to Ateles, while the use of climbing and leaping is roughly equal in the two genera. Lagothrix exhibits more generalised (primitive) locomotive behaviour in accordance with its morphology, in comparison to the more specialised Ateles. The generic differences reflect differences in habitat use and particularly foraging ecology.     

VARIABILITY OF A VESTIGIAL STRUCTURE: FIRST METACARPAL IN COLOBUS GUEREZA AND ATELES GEOFFROYI

A tenet of evolutionary theory is that, under conditions of stabilizing selection, phenotypic variability is inversely related to selection intensity. Correspondingly, a nonfunctional, vestigial structure is expected to be highly variable relative to its functional homologue. This study tests the hypothesis that species with a vestigial pollex, Colobus guereza and Ateles geoffroyi, have a first metacarpal whose length is both highly variable relative to, and poorly correlated with, the lengths of the other metapodials. The results are consistent with the hypothesis, though this combination of traits is also found in Presbytis rubicunda and Presbytis cristata. The latter two species have functional, albeit miniature, pollices. This study also demonstrates a general, inverse relationship among anthropoid primates between relative length of the first metapodial and its relative variability. These results suggest that elevated variability accompanies structural reduction.     

Locomotion of free-ranging golden lion tamarins (Leontopithecus rosalia) at the National Zoological Park

Locomotor behavior and substrate use of cage-reared golden lion tamarins (Leontopithecus rosalia), newly released and free-ranging on the grounds of the National Zoological Park, were studied to determine if locomotion changed following exposure to naturalistic conditions. The animals employed a predominantly quadrupedal locomotor profile, incorporating leaping and vertical climbing to a lesser degree. There was no clear evidence of a change in locomotion due to the high degree of variability in these behaviors. The locomotor repertoire of the free-ranging group differed from that of groups occupying unenriched but relatively large conventional enclosures, indicating that whereas locomotion is plastic with respect to environment, substrate characteristics influence locomotor behavior and may promote stereotypical behavior. However, due to anatomical constraints, the locomotor repertoire tended to be less variable than substrate use. Similar behaviors were used in moving through a variety of habitat features in spite of strong associations between specific locomotor styles and substrate classes. © 1994 Wiley-Liss, Inc.     

Locomotor behavior of Pan paniscus in Zaire

The locomotor behavior of Pan paniscus was studied over a four-week period in Equateur, Republic of Zaire. Bonobos were found to be both arboreal and terrestrial in their daily activities. In the trees adult bonobos are basically quadrupedal, but they also have significant components of armswinging, diving, leaping, and bipedalism in their locomotor repertoire.     

Locomotor behavior and skeletal morphology of two sympatric pitheciine monkeys,Pithecia pithecia and Chiropotes satanas

Field observations of two sympatric pitheciine species reveal that the positional repertoire of the white-faced saki, Pithecia pithecia, is dominated by leaping behaviors, whereas the bearded saki, Chiropotes satanas, is predominantly quadrupedal. Examination and comparison of the postcranial skeletal morphologies and limb proportions of these species display numerous features associated with their respective locomotor behaviors. These observations accord with associations found in other primate and mammalian groups and with predictions based on theoretical and experimental biomechanics. Preliminary observations of the skeletal morphology of Cacajao calvus demonstrate a marked similarity to that of Chiropotes. The fossil platyrrhine Cebupithecia sarmientoi displays greater similarity to Pithecia, suggesting that its positional repertoire also included significant leaping and clinging behaviors.     

Locomotor behavior of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park, Ecuador: general patterns and nonsuspensory modes.

Field study of the locomotor behavior of sympatric woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northern Ecuador revealed similar patterns in use of plant forms (categorized tree and liana structure), and substantial differences in the frequencies of use of different grouped modes (aggregates of kinematically similar specific modes). Lagothrix progressed more than Ateles by leaping/dropping and quadrupedal walking/running, whereas Ateles exhibited more suspensory locomotion. Grouped modes are associated with different plant forms in similar ways in the two species. In contrast, the species differed in use of tree zone (trunk/bole, major branches, intermediate branches, and terminal branches), with Lagothrix using intermediate branches and Ateles terminal branches more. Correlated with this difference was greater use by Lagothrix of quadrupedal movement, especially on intermediate branches, and greater use of suspensory modes by Ateles, especially in the terminal zone. Further research is needed to determine how these patterns are facilitated and constrained by morphological mechanisms. Analysis of specific locomotor modes within groups shows several interspecific differences in relative frequencies.     

Locomotion in captive Leontopithecus and Callimico: A multimedia study

Video studies, gait analysis, footprint tracks, and observational scan sampling show that, in comparably furnished enclosures, Leontopithecus rosalia and Callimico goeldii are superficially similar in their use of predefined locomotor patterns but differ profoundly in many underlying details which reflect differences in postcranial morphology. Each uses pronograde arboreal quadrupedal walking, quadrupedal bounding, and vertical climbing with comparable frequency, and both shift to bounding while moving quadrupedally at high speeds. In walking, both species use a diagonal sequence gait. However, in Callimico the distance per bout traveled while walking or running is shorter than in L. rosalia and there is an emphasis on leaping (from a stationary position) and bounding-leaps (saltational extensions of pronograde quadrupedalism), in contrast with the basically quadrupedal style of L. rosalia. This dichotomy is consistent with anatomical specializations, such as forelimb elongation in Leontopithecus and hindlimb elongation in Callimico. In vivo hand- and footprint studies demonstrate grasping halluces in both species while walking. Limb stances in L. rosalia during “transaxial bounding” involve an overstriding hindlimb, a predominance of oblique rather than in-line travel, and unique hand and foot positions. Anatomically, this locomotor style may be associated with reduced dexterity of the elongate hands and a relatively short hallux. The captive locomotor profiles for both species probably reflect biased samples of the locomotor repertoire of their wild counterparts. Nevertheless, these data reflect species-specific integrations of locomotor behavior and morphology, and corroborate expectations of locomotor diversity among callitrichine primates, even those of similar body size. It is suggested, however, that conventional quantitative studies of locomotor profiles may prove inadequate for resolving subtle aspects of locomotor morphology and behavior. © 1994 Wiley-Liss, Inc.     

Positional behavior,selective use of habitat substrate and associated non-positional behavior in free-rangingColobus guereza (Rüppel, 1835)

Positional behavior (posture and locomotion), associated social/maintenance behaviors and selective utilization of available habitat structure were recorded for free-rangingColobus guereza occupying a remant montane forest near Limuru, Kenya. This research design focuses on relationships between anatomy, behavior, and the environment and provides a framework for interpreting adaptations inColobus. Quantitative analyses show daily activity patterns. These monkeys spend most of their time in above branch postural activities, primarily in sitting postures. Locomotion accounts for less than one-fifth of positional behavior. In both postural and locomotor sequences, the forelimbs may be placed above the shoulder complex, often in abducted positions. Suspensory positional behavior is rare. Most activity occurs within Zone II, flexible branches of medium diameter and less than 45° in grade. Selective use of the substrate and preferred positional modes are related to variables such as social/maintenance activities, weight distribution of the link system and substrate configuration. These data suggest that, (a) black and white colobus do not exhibit behavior associated with so-called “semibrachiation” and (b) bio-behavioral adaptations involving foraging and feeding strategies may account, in part, for observed morphological differences among Old World monkeys.     

Functional anatomy of the trunk musculature in the slow loris (Nycticebus coucang)

Lorisid locomotor and postural behaviour exhibits a number of features that distinguish it clearly from other primates. The comparative myological study of the trunk in the slow loris (Nycticebus coucang) and the squirrel monkey (Saimiri sp.) presented here reveals differences that are related to unique aspects of lorisid positional behaviour. While quadrupedal running and leaping requires flexion and extension of the spine, slow climbing quadrupedalism in lorisids depends on spinal lateral flexion and rotation. The contrasting development of the epaxial musculature in the two species dissected reflects these different requirements. Bipedal suspension is a common posture in the lorisids during which rotation and dorsiflexion of the head is made possible by the robustly developed deep, dorsal, cervical musculature. The long lower lever arm in the M. rectus abdominis may play a significant role in the ventroflexion required to regain a quadrupedal stance. © 1995 Wiley-Liss, Inc.     

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.     

Locomotor behavior,body size,and comparative ecology of seven Surinam monkeys

The locomotor behavior, of seven sympatric species of New World monkeys—Saguinus midas midas, Saimiri sciureus, Pithecia pithecia, Chiropotes satanas chiropotes, Cebus apella apella, Alouatta seniculus, and Ateles paniscus panisus—was studied at the Raleighvallen-Voltzberg Nature Reserve in Central Surinam. This paper examines the way in which locomotor behavior is related to body size and to ecological parameters such as forest stratification, forest type, and diet. Locomotor behavior is clearly related to the size of the species; with increasing size, the amount of climbing increases and the amount of leaping decreases. In general, larger monkeys use larger arboreal supports; however, Saguinus midas midas uses relatively larger, and Ateles paniscus paniscus relatively smaller supports than expected from body size alone. Leaping is associated with use of the forest understory and with use of liane forest. Other types of locomotion are associated with main canopy use in a variety of forest types. There are no consistent associations between diet and either locomotor behavior or forest utilization; rather, monkeys with similar diets show locomotor and habitat differentiation.     

The locomotor behavior of Callicebus brunneus and Callicebus torquatus

This study presents data on the positional behavior of Callicebus torquatus and Callicebus brunneus collected from two different localities in Peru. C. brunneus primarily utilizes short-distance, bounding leaps, while C. torquatus relies predominantly on quadrupedal walking. Both species utilize small, horizontal and terminal branches more than any other substrate class. We relate the differences in locomotor behaviors between the two species to their utilization of different forest levels. C. brunneus tends to reside in the understory and brush layer forest levels. These more discontinuous strata necessitate higher frequencies of short-distance leaping. C. torquatus occupies the more continuous, interconnected canopy level, and much of its food is found in this level. Comparisons with other species show that Callicebus spp. locomote along smaller-sized, horizontal branches using quadrupedal progression and leaping.     

Digestibility of a high-fiber biscuit-based diet by black and white colobus (Colobus guereza)

The acceptability and digestibility of a high-fiber biscuit-based diet was investigated using two adult male Colobus guereza animals. Although the animals were initially reluctant to accept the biscuit, it was eventually readily consumed. Apparent digestion coefficients for the diet (average composition, dry matter basis: 16% crude protein, 25% neutral detergent fiber (NDF), 9.5% acid detergent fiber (ADF), 1.2% acid lignin) determined by total fecal collection were 0.871 for dry matter, 0.813 for NDF, 0.693 for ADF, and 0.208 for acid lignin. Fiber digestive capabilities in C. guereza generally exceeded those reported in ruminant species based on predictive equations. Use of acid lignin and Cr₂O₃ as markers underestimated dry matter digestibility by 3.9 and 6.0%, respectively.     

Knuckle walking signal in the manual digits of Pan and Gorilla

This article examines the curvature of the manual proximal and middle phalanges of species belonging to Pan, Gorilla, Ateles, Macaca, Pongo, Hylobates, and Cebus to determine whether middle phalangeal curvature, when considered in conjunction with proximal phalangeal curvature, yields a locomotor signal. Prior studies have demonstrated the discriminatory power of proximal phalanges for separating suspensory species (including knuckle walkers) from pronograde quadrupedal species, but less emphasis has been placed on the distinguishing phalangeal characteristics of taxa within the suspensory category. This study demonstrates, first, that middle phalanges discriminate suspensory from nonsuspensory species, although not as cleanly as proximal phalanges. Finer discrimination of locomotor signals, including subtle differences among animals employing different modes of suspension, is possible through a comparison of the curvatures of the proximal phalanges and corresponding middle phalanges. Their relative curvature differs in quadrupeds, brachiators, and knuckle walkers. Knuckle walkers (Pan and Gorilla) have relatively little curvature of the middle phalanges coupled with marked curvature of the proximal phalanges, whereas brachiators (Ateles and Hylobates) display marked curvature of both proximal and middle phalanges, and pronograde quadrupeds (Cebus and Macaca) have relatively straight proximal and moderately curved middle phalanges. Quadrumanous climbers (Pongo) have a unique combination of traits, whereby curvature is high in both proximal and middle phalanges, but less so in the latter than the former. These differences, predictable on the basis of the biomechanical forces to which digits are subjected, may open a new venue for future research on the locomotor repertoire of prebipedal ancestors of hominins.     

A comparative study of positional behavior in three species of tamarin monkeys

Tamarins of the genusSaguinus are small-bodied New World monkeys that exhibit clawlike or modified nails. Patterns of positional behavior and habitat utilization are presented for three species,Saguinus fuscicollis, S. geoffroy, andS. mystax. These data were collected on free-ranging tamarin populations in Panama and Peru. Despite considerable differences in body weight, all three species exhibited very similar patterns of positional behavior, with quadrupedal bounding and running accounting for 43 – 52% of travel time. Leaping was the second most common locomotor activity and accounted for 31 – 41% of travel. Although each species leaped principally on small supports in the perimeter of the tree crown, approximately 20% of all leaps inS. fuscicollis involved moderate to large sized vertical trunks located in the undercanopy. Leaping between trunks was rare in the two larger tamarin species. Measurements taken on live wild-trapped adults reveal that compared toSaguinus geoffroyi andS. mystax, S. fuscicollis is characterized by a long legspan and an especially long armspan. It is proposed that inS. fuscicollis, elongated forelimbs play an important role in maneuvering and rotating the body during the in-air phase of trunk-to-trunk leaping, and increase the breaking distance needed to decelerate the body upon impact. Additional relationships between body size, substrate preference, and positional behavior in callitrichines are discussed.     

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.     

Gustatory Responsiveness to food-associated acids in the spider monkey (Ateles geoffroyi)

The gustatory responsiveness of four adult spider monkeys to five food-associated acids was assessed in two-bottle preference tests of brief duration (3 min). The animals were given the choice between a 30 mM sucrose solution and defined concentrations of citric acid, ascorbic acid, malic acid, acetic acid, or tannic acid dissolved in a 30 mM sucrose solution. With this procedure,Ateles geoffroyi was found to significantly discriminate concentrations as low as 5 mM ascorbic acid, citric acid, and acetic acid, 10 mM malic acid, and 0.1 mM tannic acid from the alternative stimulus. With the latter two substances, the monkeys rejected all suprathreshold concentrations tested, whereas with the former three substances, the animals showed an inverted U-shaped function of preference, i.e. they rejected high concentrations, but significantly preferred low but detectable concentrations of these acidic tastants over the alternative sweet stimulus. The results showed (1) the spider monkey to respond to the same range of acid concentrations as other nonhuman primate species; (2) thatAteles geoffroyi, is able to detect food-associated acids at concentrations well below those present in most fruits; and (3) that unlike most other primate species tested so far, spider monkeys do not generally reject acidic tastants but show a substanceand concentration-dependent change in responsiveness that may range from rejection to preference. The results support the assumptions that spider monkeys may use sourness and/or astringency of food-associated acids as a criterion for food selection, and that the gustatory responsiveness ofAteles geoffroyi to acidic tastants might reflect an evolutionary adaptation to frugivory.     

Gustatory thresholds for food-associated sugars in the spider monkey (Ateles geoffroyi)

The purpose of this study was to determine gustatory thresholds for five different food-associated sugars in Ateles geoffroyi. Using a two-bottle test, three adult spider monkeys were found to significantly prefer concentrations as low as 3 mM sucrose, 15 mM fructose, 20 mM glucose, and 10 mM lactose over tap water. Maltose was significantly discriminated down to 20 mM with individual animals showing either a preference or an aversion, or an inverted U-shaped function of preference toward higher concentrations of this carbohydrate. The results showed the spider monkey to respond to lower sugar concentrations compared to other nonhuman primates tested so far and thus support the assumptions that Ateles geoffroyi may use sweetness as a criterion for food selection, and that the remarkably high sweet-taste sensitivity of this frugivorous species might be correlated with its dietary specialization. © 1996 Wiley-Liss, Inc.