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.     

Suspensory locomotion of Lagothrix lagothricha and Ateles belzebuth in Yasuní National Park,Ecuador

A comparative field study of the locomotion of woolly monkeys (Lagothrix lagothricha) and spider monkeys (Ateles belzebuth) in undisturbed rainforest of northeastern Ecuador reveals substantial differences in their use of suspensory modes. Ateles performed both more brachiation (by forelimbs and tail, with trunk rotation), and forelimb swing (similar to brachiation, but without trunk rotation) than Lagothrix. In contrast, in Lagothrix 20% of suspensory movement was by pronograde forelimb swing, which resembles forelimb swing except that the body is held in a pronograde orientation due to the tail and/or feet intermittently grasping behind the trailing forelimb. Ateles never exhibited this mode. Both brachiation and forelimb swing by Ateles were more dynamic than in Lagothrix, consisting of higher proportions of full-stride bouts (versus single-step). Both species used smaller supports for suspensory than for quadrupedal locomotion, and Ateles used both smaller and larger supports for suspension than did Lagothrix. Analysis of support inclination shows that both species tended to perform more above-support movement on horizontal supports and more below-support (suspensory) movement from oblique supports. Our attempt to elucidate the aspects of canopy structure that favor suspension suggests the need for additional kinds of observational data, focusing on the "immediate structural context" of positional events.     

Role of the prehensile tail during ateline locomotion: experimental and osteological evidence

The dynamic role of the prehensile tail of atelines during locomotion is poorly understood. While some have viewed the tail of Ateles simply as a safety mechanism, others have suggested that the prehensile tail plays an active role by adjusting pendulum length or controlling lateral sway during bimanual suspensory locomotion. This study examines the bony and muscular anatomy of the prehensile tail as well as the kinematics of tail use during tail-assisted brachiation in two primates, Ateles and Lagothrix. These two platyrrhines differ in anatomy and in the frequency and kinematics of suspensory locomotion. Lagothrix is stockier, has shorter forelimbs, and spends more time traveling quadrupedally and less time using bimanual suspensory locomotion than does Ateles. In addition, previous studies showed that Ateles exhibits greater hyperextension of the tail, uses its tail to grip only on alternate handholds, and has a larger abductor caudae medialis muscle compared to Lagothrix. In order to investigate the relationship between anatomy and behavior concerning the prehensile tail, osteological data and kinematic data were collected for Ateles fusciceps and Lagothrix lagothricha. The results demonstrate that Ateles has more numerous and smaller caudal elements, particularly in the proximal tail region. In addition, transverse processes are relatively wider, and sacro-caudal articulation is more acute in Ateles compared to Lagothrix. These differences reflect the larger abductor muscle mass and greater hyperextension in Ateles. In addition, Ateles shows fewer side-to-side movements during tail-assisted brachiation than does Lagothrix. These data support the notion that the prehensile tail represents a critical dynamic element in the tail-assisted brachiation of Ateles, and may be useful in developing inferences concerning behavior in fossil primates.     

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.     

Atelinae adaptations: behavioral strategies and ecological constraints.

Comparisons between the four genera that make up the Atelinae reveal two distinct behavioral patterns, one in which energy expenditure is minimized (Alouatta) and one in which energy intake is maximized (Lagothrix, Ateles, and Brachyteles). Among the atelins, Lagothrix and Ateles devote over 75% of their annual feeding time to fruit, while Brachyteles devotes between 50% and 67% of their feeding time to leaves. Pronounced seasonality in the Atlantic coastal forest inhabited by Brachyteles may be responsible for its more folivorous diet. Alouatta falls in the body size range of Lagothrix and is much smaller than Ateles and Brachyteles. Nonetheless, Alouatta is more folivorous than sympatric atelins. The atelins also share a rapid, suspensory mode of locomotion that appears to enable them to minimize travel time between widely dispersed fruit sources. Alouatta, by contrast, employs a slower, but more energetically efficient, quadrupedal locomotion. Ranging patterns among the Atelinae are consistent with both diet and locomotor abilities: Atelins travel daily distances up to 5,000 m; Alouatta ranges are much shorter. Further distinctions are evident in Atelinae grouping patterns. Alouatta remains in small cohesive groups that occupy home ranges less than 60 ha in size. Both Lagothrix and Ateles have large groups that fission to reduce the costs of intragroup feeding competition when preferred fruits occur in small patches within much larger community ranges. While greater reliance on low-energy foods such as leaves may release Brachyteles from similar competitive constraints, their tendency toward fluid grouping associations is consistent with the pursuit of a frugivorous diet.     

The ecological role of the prehensile tail in white-faced capuchins (Cebus capucinus).

Prehensile tails appear to have evolved at least twice in platyrrhine evolution. In the atelines, the tail is relatively long and possesses a bare area on the distal part of its ventral surface that is covered with der-matoglyphs and richly innervated with Meissner's corpuscles. In contrast, the prehensile tail of Cebus is relatively short, fully haired, and lacks specialized tactile receptors. Little is currently known regarding tail function in capuchins, and whether their prehensile tail serves a greater role in feeding or traveling. In this paper we examine patterns of positional behavior, substrate preference, and tail use in wild white-faced capuchins (Cebus capucinus) inhabiting a wet tropical forest in northeastern Costa Rica. Observational data were collected over the course of 3 months on adult capuchins using an instantaneous focal animal time sampling technique. Differences in the frequency and context of tail use, and the estimated amount of weight support provided by the tail relative to other appendages during feeding/foraging and traveling were used as measures of the ecological role of this specialized organ in capuchin positional behavior. During travel, quadrupedal walking, leaping, and climbing dominated the capuchin positional repertoire. The capuchin tail provided support in only 13.3% of travel and was principally employed during below branch locomotor activities. In contrast, tail-assisted postures accounted for 40.6% of all feeding and foraging records and occurred primarily in two contexts. The tail was used to suspend the individual below a branch while feeding, as well as to provide leverage and weight support in above-branch postures associated with the extraction of prey from difficult to search substrates. A comparison of tail use in Cebus, with published data on the atelines indicates that both taxa possess a grasping tail that is capable of supporting the animal's full body weight. In capuchins and howling monkeys, the tail appears to be used more frequently and serves a greater weight-bearing role during feeding than during traveling. In Ateles, and possibly Brachyteles, and Lagothrix, however, the prehensile tail serves a dual role in both feeding and forelimb suspensory locomotion. Additional relationships between white-faced capuchin feeding, positional behavior, extractive foraging techniques, and prehensile tail use are discussed.     

Locomotion and feeding postures of spider and howling monkeys: field study and evolutionary interpretation

Field observations demonstrate clear differences in locomotion and feeding postures between spider monkeys (Ateles) and howling monkeys (Alouatta). When feeding, Ateles employs sitting postures approximately half the time, and a variety of suspensory postures using the tail the other half. Ateles moves quadrupedally during 52% of locomotion, by tail-arm suspension 25%, and various mixed support-suspensory modes the remainder. Tail-arm suspension is practiced more rapidly on thinner supports, and on more negatively inclined supports than is quadrupedal movement. Howlers do not locomote by tail-arm suspension: movement is almost entirely quadrupedal and is slower than that of spider monkeys. The positional behavior of spider monkeys fits closely recent views of major adaptive changes in hominoid evolution emphasizing brachiation and speed during travel. Howler locomotion and also tissue composition appear related to diet and digestive mechanisms.     

The locomotor and postural repertoires of Ateles geoffroyi and Colobus guereza,and a reevaluation of the locomotor category semibrachiation

The locomotor repertoire of Ateles geoffroyi includes quadrupedal walking and running, climbing, brachiation and arm-swinging, bipedalism, and leaping. Its postural repertoire is characterized by below branch suspensory activities. In contrast, the locomotor repertoire of Colobus guereza consists primarily of quadrupedal galloping and bounding, and leaping. It does not brachiate or walk bipedally and rarely performs arm-swinging. The Colobus guereza postural repertoire is characterized by above branch sitting postures. Ateles geoffroyi is a highly mobile primate, whereas Colobus guereza is essentially sedentary. In the past, there has been a tendency to group Ateles and Colobus in a single locomotor category, semibrachiation. Comparison of the very different repertoires of these two species points out some of the shortcomings of the category semibrachiation. First, no locomotor pattern or group of patterns has been described as semibrachiation (i.e., no animals semibrachiate). Secondly, the locomotor diversity of animals included in the category is so much greater than the similarities that the category obscures more than it conveys. The usefulness of retaining this category is therefore questioned.     

Party size and diet of syntopic atelids (Ateles chamek and Lagothrix cana) in Southwestern Brazilian Amazonia.

Syntopic Alouatta seniculus, Ateles chamek and Lagothrix cana (Atelidae) were studied in southwestern Amazonia. Primate populations were first surveyed, and then the party size, diet and vertical spacing were monitored over a 5-month period. Atelids accounted for more than half the survey sightings and Lagothrix was the most abundant. Party sizes recorded for both Alouatta and Lagothrix during monitoring were significantly larger than those recorded during surveys, but no such difference was found for Ateles. Monitored parties were significantly larger in Lagothrix in comparison with either Alouatta or Ateles, as were groups of Ateles in comparison with Alouatta. Mean party size in Ateles decreased progressively during the course of the study, from 8.9 +/- 3.4 in June to 3.9 +/- 2.3 in October. Moraceae was the most important dietary resource for Ateles and Lagothrix, in terms of both feeding records and number of species exploited. There was considerable overlap in the plant taxa exploited, but some notable differences, such as the exclusive use of Hymenaea courbaril (Caesalpinaceae) by Lagothrix and of Euterpe precatoria (Arecaceae) by Ateles. As at other sites in the region, Ateles occupied significantly higher forest strata in comparison with Lagothrix. Despite the preliminary nature of the study, the results indicate a number of ecological differences between species that undoubtedly play an important role in niche separation.     

Photopigments and colour vision in New World monkeys from the family Atelidae

Most New World monkeys have an X-chromosome opsin gene polymorphism that produces a variety of different colour vision phenotypes. Howler monkeys (Alouatta), one of the four genera in the family Atelidae lack this polymorphism. Instead, they have acquired uniform trichromatic colour vision similar to that of Old World monkeys, apes and people through opsin gene duplication. In order to determine whether closely related monkeys share this arrangement, spectral sensitivity functions that allow inferences about cone pigments were measured for 56 monkeys from two other Atelid genera, spider monkeys (Ateles) and woolly monkeys (Lagothrix). Unlike howler monkeys, both spider and woolly monkeys are polymorphic for their middle- and long-wavelength cone photopigments. However, they also differ from other polymorphic New World monkeys in having two rather than three possible types of middle- and long-wavelength cone pigments. This feature directly influences the relative numbers of dichromatic and trichromatic monkeys.     

Polymorphism of visual pigment genes in the muriqui (Primates, Atelidae)

Colour vision varies within the family Atelidae (Primates, Platyrrhini), which consists of four genera with the following cladistic relationship: {Alouatta[Ateles (Lagothrix and Brachyteles)]}. Spider monkeys (Ateles) and woolly monkeys (Lagothrix) are characteristic of platyrrhine monkeys in possessing a colour vision polymorphism. The polymorphism results from allelic variation of the single-locus middle-to-long wavelength (M/L) cone opsin gene on the X-chromosome. The presence in the population of alleles coding for different M/L photopigments results in a variety of colour vision phenotypes. Such a polymorphism is absent in howling monkeys (Alouatta), which, alone among platyrrhines, acquired uniform trichromatic vision similar to that of Old World monkeys, apes, and humans through opsin gene duplication. Dietary and morphological similarities between howling monkeys and muriquis (Brachyteles) raise the possibility that the two genera share a similar form of colour vision, uniform trichromacy. Yet parsimony predicts that the colour vision of Brachyteles will resemble the polymorphism present in Lagothrix and Ateles. Here we test this assumption. We obtained DNA from the blood or faeces of 18 muriquis and sequenced exons 3 and 5 of the M/L opsin gene. Our results affirm the existence of a single M/L cone opsin gene in the genus Brachyteles. We detected three alleles with predicted lambdamax values of 530, 550, and 562 nm. Two females were heterozygous and are thus predicted to have different types of M/L cone pigment. We discuss the implication of this result towards understanding the evolutionary ecology of trichromatic vision.     

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.     

Trabecular bone structure in the primate wrist

Trabecular (or cancellous) bone has been shown to respond to mechanical loading throughout ontogeny and thus can provide unique insight into skeletal function and locomotion in comparative studies of living and fossil mammalian morphology. Trabecular bone of the hand may be particularly functionally informative because the hand has more direct contact with the substrate compared with the remainder of the forelimb during locomotion in quadrupedal mammals. This study investigates the trabecular structure within the wrist across a sample of haplorhine primates that vary in locomotor behaviour (and thus hand use) and body size. High‐resolution microtomographic scans were collected of the lunate, scaphoid, and capitate in 41 individuals and eight genera (Homo, Gorilla, Pan, Papio, Pongo, Symphalangus, Hylobates, and Ateles). We predicted that particular trabecular parameters would 1) vary across suspensory, quadrupedal, and bipedal primates based on differences in hand use and load, and 2) scale with carpal size following similar allometric patterns found previously in other skeletal elements across a larger sample of mammals and primates. Analyses of variance (trabecular parameters analysed separately) and principal component analyses (trabecular parameters analysed together) revealed no clear functional signal in the trabecular structure of any of the three wrist bones. Instead, there was a large degree of variation within suspensory and quadrupedal locomotor groups, as well as high intrageneric variation within some taxa, particularly Pongo and Gorilla. However, as predicted, Homo sapiens, which rarely use their hands for locomotion and weight support, were unique in showing lower relative bone volume (BV/TV) compared with all other taxa. Furthermore, parameters used to quantify trabecular structure within the wrist scale with size generally following similar allometric patterns found in trabeculae of other mammalian skeletal elements. We discuss the challenges associated with quantifying and interpreting trabecular bone within the wrist. J. Morphol. 275:572–585, 2014. © 2013 Wiley Periodicals, Inc.     

Arboreal locomotor and postural behaviour of European red squirrels (<Emphasis Type="Italic">Sciurus vulgaris</Emphasis> L.) in northern Greece

The study of the locomotion and postures of arboreal squirrels may provide important contextual information on the evolution of the morphology and ecology of sciurids. In this context, we studied the positional behaviour and habitat use of four adult European red squirrels (Sciurus vulgaris L.) in a mixed coniferous forest in northern Greece. Our results show that, during the study period, S. vulgaris extensively used the forest canopy and the terminal branch zone. The use of small and medium supports of all orientations was also particularly frequent. The positional profile of the species was characterized by the dominance of quadrupedal, clawed and airborne locomotion along with seated and standing postures. Quadrupedalism and sitting appeared to promote terminal branch use for food access and manipulation, while claw climbing favored vertical ranging and retreat to trees after terrestrial foraging. Finally, leaping reduced energetic costs during travelling between food sites within the relatively dispersed forest. These results and those of previous research on the positional behaviour of other squirrels reveal several trends related to body size, arboreal or gliding habits and tropical or temperate forest distribution and contribute to the understanding of evolutionary novelty in multiple levels within the sciurid radiation.     

Locomotor and postural behavior in Alouatta palliata and Cebus capucinus

Positional behavior of two platyrrhine monkeys, Alouatta palliata and Cebus capucinus, was observed at La Pacifica and Santa Rosa National Park, Costa Rica. Frequency data for locomotion, postures, support diameters, orientation of supports, and use of canopy were recorded on focal males and females. Alouatta palliata is a frequent user of arboreal quadrupedalism (47%) and climbing (37%), with bridging (10%) representing the next most frequent type of locomotion. Intraspecific comparisons show the smaller-sized females of Alouatta to prefer very small diameter supports, the lower canopy, and to climb more frequently than the larger males—a pattern opposite to that which has been documented to occur with increasing body size across species. A more limited study on Cebus capucinus shows this species to be highly quadrupedal (54%) with moderately high locomotor frequencies for climbing (26%) and leaping (15%).     

Positional Behavior of Cercopithecus petaurista

I studied the positional behavior and habitat use of Cercopithecus petaurista, the lesser spot-nosed monkey, in the Ivory Coast's Taï Forest for 15 months. I compare these data with similar information collected on sympatric groups of Cercopithecus diana and C. campbelli in order to examine further the relationships between locomotion, posture, support use, stratal use, body size, diet, activity patterns and foraging behavior. Spot-nosed monkeys are predominantly quadrupedal primates that frequent the top layer of the understory during all maintenance activities. Locomotion is characteristically slow and cautious; travel takes place on branches and boughs while foraging occurs on twigs and branches. Postural behavior of Cercopithecus petaurista reflects their reliance on more ubiquitously distributed, less mobile food items. The relationship between body size, climbing, leaping and support use among Taï guenons is weak; interspecific differences are more likely functions of strata use and overall behavioral characteristics, e.g. crypticity. I also compare the locomotion and support use of Cercopithecus petaurista with that of C. ascanius from Uganda's Kibale Forest (Gebo and Chapman, 1995a) in order to assess the behavioral similarity of members of the same superspecies. Although overall support use is quite similar, the monkeys differ significantly in frequencies of quadrupedism, leaping and climbing. I present possible reasons for and implications of these differences.     

Telemetered electromyography of flexor digitorum profundus and flexor digitorum superficialis in Pan troglodytes and implications for interpretation of the O. H. 7 hand.

The importance of knuckle-walking in the locomotor repertoire of African apes raises the possibility that the long digital flexors may be specially adapted more to meet the demands of ground quadrupedalism than those of suspension. To investigate this possibiltiy, the activities of the flexor digitorum superficialis and flexor digitorum profundus were studied by means of telemetered electromyography in three chimpanzees. Results clearly indicate that the fasciculi of the muscles to digits bearing weight in knuckle-walking are not called upon to contract in quadrupedal postures or in slow and moderately fast quadrupedal locomotion except to help clear the fingers from the ground as the forelimb begins its recovery stroke. At the most rapid speeds, a slight to moderate level of activity sometimes occurs in the latter half of stance phase. The long digital flexors display maximum and sustained activity during suspension. It is concluded that any role for these muscles in maintenance of stability at the metacarpophalangeal joints during knuckle-walking must be predominantly passive. Prominent markings for insertions of these muscles in a fossil hand (such as O.H. 7) suggest use of the forelimb in suspensory climbing behaviors.     

Molecular phylogeny of ateline new world monkeys (Platyrrhini, atelinae) based on gamma-globin gene sequences: evidence that brachyteles is the sister group of lagothrix

Nucleotide sequences, each spanning approximately 7 kb of the contiguous gamma1 and gamma2 globin genomic loci, were determined for seven species representing all extant genera (Ateles, Lagothrix, Brachyteles, and Alouatta) of the New World monkey subfamily Atelinae. After aligning these seven ateline sequences with outgroup sequences from several other primate (non-ateline) genera, they were analyzed by maximum parsimony, maximum likelihood, and neighbor-joining algorithms. All three analyzes estimated the same phylogenetic relationships: [Alouatta [Ateles (Brachyteles, Lagothrix)]]. Brachyteles and Lagothrix are sister-groups supported by 100% of bootstrap replications in the parsimony analyses. Ateles joins this clade, followed by the basal genus Alouatta; these joinings were strongly supported, again with 100% bootstrap values. This cladistic pattern for the four ateline genera is congruent with that obtained in previous studies utilizing epsilon-globin, IRBP, and G6PD nuclear genomic sequences as well as mitochondrial COII sequences. Because the number of aligned nucleotide positions is much larger in the present datasetoff than in any of these other datasets, much stronger support was obtained for the cladistic classification that divides subfamily Atelinae into tribes Alouattini (Alouatta) and Atelini, while the latter divides into subtribes Atelina (Ateles) and Brachytelina (Brachyteles and Lagothrix).     

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.