The effect of branch diameter on primate gait sequence pattern

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

Positional information and pattern formation

Spatial patterns of cellular differentiation may arise from cells first being assigned a position, as in a coordinate system, and then interpreting the positional value that they have acquired. This interpretation will depend on their genetic constitution and developmental history. Different patterns may thus arise from similar positional fields. The specification of positional value may involve a positional signal, such as the concentration of a diffusible morphogen, but can also depend on how long the cells remain in a particular region, such as a progress zone. Positional values may also be acquired by direct transfer from one cell layer to another, as in directed embryonic induction. Positional value, unlike a positional signal, involves long-term memory, and can be regarded as a type of cell determination. Cells of the same differentiation class may have different positional values and may thus be non-equivalent. Evidence is presented for a signal providing positional information along the antero-posterior axis during chick limb development. This signal has properties similar to those of a diffusible morphogen.     

Stability of positional identity of axolotl blastema cells in vitro

Summary Previous grafting experiments have demonstrated that cells from non-contiguous positions within developing and regenerating limbs differ in a property referred to as positional identity. The goal of this study was to determine how long the positional identity of axolotl limb blastema cells is stable during culture in vitro. We have developed an assay for posterior positional properties such that blastema cells can be cultured and then grafted into anterior positions in host blastemas, to determine if they can stimulate supernumerary digit formation. We report that posterior blastema cells are able to maintain their positional identities for at least a week in culture. In addition, we observed that blastema cells are able to rapidly degrade collagenous substrates in vitro, a property that apparently distinguishes them from limb cells of other vertebrates. These results provide information regarding the time boundaries within which the positional properties of blastema cells can be studied and manipulated in vitro. Correspondence to: S.V. Bryant     

Balancing costs and benefits in primates: ecological and palaeoanthropological views

Maintaining the balance between costs and benefits is challenging for species living in complex and dynamic socio-ecological environments, such as primates, but also crucial for shaping life history, reproductive and feeding strategies. Indeed, individuals must decide to invest time and energy to obtain food, services and partners, with little direct feedback on the success of their investments. Whereas decision-making relies heavily upon cognition in humans, the extent to which it also involves cognition in other species, based on their environmental constraints, has remained a challenging question. Building mental representations relating behaviours and their long-term outcome could be critical for other primates, but there are actually very little data relating cognition to real socio-ecological challenges in extant and extinct primates. Here, we review available data illustrating how specific cognitive processes enable(d) modern primates and extinct hominins to manage multiple resources (e.g. food, partners) and to organize their behaviour in space and time, both at the individual and at the group level. We particularly focus on how they overcome fluctuating and competing demands, and select courses of action corresponding to the best possible packages of potential costs and benefits in reproductive and foraging contexts.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

Ontogeny of limb mass distribution in infant baboons (Papio cynocephalus)

Primates have more distally distributed limb muscle mass compared to most nonprimate mammals. The heavy distal limbs of primates are likely related to their strong manual and pedal grasping abilities, and interspecific differences in limb mass distributions among primates are correlated with the amount of time spent on arboreal supports. Within primate species, individuals at different developmental stages appear to differ in limb mass distribution patterns. For example infant macaques have more distally distributed limb mass at young ages. A shift from distal to proximal limb mass concentrations coincides with a shift from dependent travel (grasping their mother's hair) to independent locomotion. Because the functional demands placed on limbs may differ between taxa, understanding the ontogeny of limb mass distribution patterns is likely an essential element in interpreting the diversity of limb mass distribution patterns present in adult primates. This study examines changes in limb inertial properties during ontogeny in a longitudinal sample of infant baboons (Papio cynocephalus). The results of this study show that infant baboons undergo a transition from distal to proximal limb mass distribution patterns. This transition in limb mass distribution coincides with the transition from dependent to independent locomotion during infant development. Compared to more arboreal macaques, infant baboons undergo a faster transition to more proximal limb mass distribution patterns. These results suggest that functional demands placed on the limbs during ontogeny have a strong impact on the development of limb mass distribution patterns.     

Positional behavior and body size of arboreal primates: a theoretical framework for field studies and an illustration of its application.

The rationale for most field studies of the positional behavior of arboreal primates has been the need to document natural behaviors quantitatively in order to infer the functional significance of morphological configurations. This focus on interactions of morphology with behavior is justifiable, but there exists another important level of biological relationships, that of the animal with its structural habitat, which it must negotiate to find food and avoid being preyed on. Recently it has become apparent that body size is likely to affect relationships of positional behavior with habitat structure, as well as with morphology. Here I offer a framework for research on functional relationships of positional behavior, body size, and habitat structure, with the ultimate objective of elucidating the aptive significance of the great diversity exhibited by arboreal primates. This approach specifies several distinct problems that animals solve, and indicates how research might be directed at revealing the relative effectiveness with which different primates solve them. A preliminary application of the framework examines sympatric north Sumatran primates.     

The functional morphology of weight bearing: limb joint surface area allometry in anthropoid primates

Biomechanical scaling of long bone joint surface areas was investigated in 13 species of anthropoid primates. It was proposed that joint surface areas should scale with positive allometry with respect to body size in order to maintain relatively constant safety factors for joints in small and large animals and that modifications from the overall pattern of scaling may be expected in the limb joints of species exhibiting specialized locomotor behaviours that radically alter limb loading. Within anthropoids, the brachiating primates, white-handed gibbons ( Hylobates lar ) and black-handed spider monkeys ( Ateles geoffroyi ), were used to test this hypothesis. Total joint surface areas were found to scale with significant positive allometry in 11 of 12 limb joints. The observed pattern of interspecific allometry supports the hypothesis that weight bearing is a major constraint on the design of joints. This positive interspecific allometry is reflected at the intraspecific level as well, with larger joints of larger species showing significant intraspecific scaling. Suspensory species showed no significant deviations from the overall anthropoid pattern, despite their reduced compressive loading of the limb joints, even after controlling for joint mobility. These results suggest that, while evolutionary changes in locomotor behaviour that produce significant increases in loading of a joint may be accompanied by selection for increased joint surface areas, adoption of locomotor repertoires that reduce limb loading may have no selective effect on joint morphology, and joint design in these cases will reflect the biomechanics of the ancestral locomotor condition.     

The Ontogeny of Prehensile‐Tail Use in Cebus capucinus and Alouatta palliata

A study of the platyrrhine prehensile tail provides an opportunity to better understand how ecological and biomechanical factors affect the ability of primates to distribute mass across many different kinds of arboreal supports. Young individuals experience ontogenetic changes in body mass, limb proportions, and motor skills that are likely to exert a strong influence on foraging strategies, social behaviors, support use, and associated prehensile‐tail use. In this research, I examine ontogenetic patterns of prehensile‐tail use in Cebus capucinus and Alouatta palliata. I collected behavioral data on activity, positional context, support size, and prehensile‐tail use in five age categories of white‐faced capuchins and mantled howlers during a 12‐month period at Estación Biológica La Suerte in northeastern Costa Rica. Infant and juvenile howlers and capuchins were found to use their prehensile tails significantly more often than adults during feeding, foraging, and social behavior. Prehensile‐tail use did not show predictable increases during growth. In both species, adults used their prehensile tails in mass‐bearing modes significantly less often than juveniles. Despite differences in tail anatomy in Cebus and Alouatta, prehensile‐tail use was observed to follow an increasing trajectory from infancy, peaking during juvenescence, and then decreasing in older juveniles and adults. In both species, it appeared that adult patterns of prehensile‐tail use reflected the demands placed on young juveniles. Am. J. Primatol. 74:770‐782, 2012. © 2012 Wiley Periodicals, Inc.     

Positional behavior in five sympatric old world monkeys

Observations of positional behavior and habitat use were recorded on focal individuals of five species of Old World monkeys at Kibale Forest, Uganda, through the dry season of 1990 and 1991. Cercopithecus ascanius, Cercopithecus mitis, Cercocebus albigena, Colobus badius, and Colobus guereza commonly utilize five similar types of positional behavior (i.e., quadrupedalism, leaping, climbing, sitting, and standing), but in varying frequencies and situations. As a group, colobines use oblique supports and leap more often, and cover greater linear distances during leaps than do cercopithecines. Colobines also prefer to sit (about 90% of all postures), while cercopithecines stand more frequently. Body size differences between the sexes of a species are not reflected in positional behavior. The two small-bodied species climb more and leap less often than the three larger species, which is the reverse of what we would expect. Leaping is the most common method of crossing open spaces within the canopy; but most spatial gaps and leaps are over short distances, usually one meter or less. All five species, regardless of body size or the availability of forest supports, prefer mediumsized supports. Incorporating our work from Uganda with previous investigations of positional behavior reveals few consistent trends with respect to body size or habitat use across primates. © 1995 Wiley-Liss, Inc.     

A dynamic force analysis system for climbing of large primates

Registering substrate reaction forces from primates during climbing requires the design and construction of customized recording devices. The technical difficulties in constructing a reliable apparatus hinder research on the kinetics of primate locomotion. This is unfortunate since arboreal locomotion, especially vertical climbing, is an important component of the hominoid locomotor repertoire. In this technical paper, we describe a custom-built climbing pole that allows recordings of dynamic 3-dimensional forces during locomotion on horizontal and sloping substrates and during vertical climbing. The pole contains an instrumented section that can readily be modified and enables us to register forces of a single limb or multiple limbs in a broad range of primates. For verification, we constructed a similar set-up (which would not be usable for primates) using a conventional force plate. Data for a human subject walking on both set-ups were compared. The experimental set-up records accurate and reliable substrate reaction forces in three orthogonal directions. Because of its adjustability, this type of modular set-up can be used for a great variety of primate studies. When combining such kinetic measurements together with kinematic information, data of great biomechanical value can be generated. These data will hopefully allow biological anthropologists to answer current questions about primate behaviours on vertical substrates.     

Non-human primate token use shows possibilities but also limitations for establishing a form of currency

Non-human primates evaluate choices based on quantitative information and subjective valuation of options. Non-human primates can learn to value tokens as placeholders for primary rewards (such as food). With those tokens established as a potential form of ‘currency’, it is then possible to examine how they respond to opportunities to earn and use tokens in ways such as accumulating tokens or exchanging tokens with each other or with human experimenters to gain primary rewards. Sometimes, individuals make efficient and beneficial choices to obtain tokens and then exchange them at the right moments to gain optimal reward. Sometimes, they even accumulate such rewards through extended delay of gratification, or through other exchange-based interactions. Thus, non-human primates are capable of associating value to arbitrary tokens that may function as currency-like stimuli, but there also are strong limitations on how non-human primates can integrate such tokens into choice situations or use such tokens to fully ‘symbolize’ economic decision-making. These limitations are important to acknowledge when considering the evolutionary emergence of currency use in our species.This article is part of the theme issue ‘Existence and prevalence of economic behaviours among non-human primates’.     

The Impact of Cognitive Testing on the Welfare of Group Housed Primates

Providing cognitive challenges to zoo-housed animals may provide enriching effects and subsequently enhance their welfare. Primates may benefit most from such challenges as they often face complex problems in their natural environment and can be observed to seek problem solving opportunities in captivity. However, the extent to which welfare benefits can be achieved through programmes developed primarily for cognitive research is unknown. We tested the impact of voluntary participation cognitive testing on the welfare of a socially housed group of crested macaques (Macaca nigra) at the Macaque Study Centre (Marwell Zoo). First, we compared the rate of self-directed and social behaviours on testing and non-testing days, and between conditions within testing days. Minimal differences in behaviour were found when comparing testing and non-testing days, suggesting that there was no negative impact on welfare as a result of cognitive testing. Lipsmacking behaviours were found to increase and aggressive interaction was found to decrease in the group as a result of testing. Second, social network analysis was used to assess the effect of testing on associations and interactions between individuals. The social networks showed that testing subjects increased their association with others during testing days. One interpretation of this finding could be that providing socially housed primates with an opportunity for individuals to separate from the group for short periods could help mimic natural patterns of sub-group formation and reunion in captivity. The findings suggest, therefore, that the welfare of captive primates can be improved through the use of cognitive testing in zoo environments.     

Hip extensor EMG and forelimb/hind limb weight support asymmetry in primate quadrupeds

Higher weight support on the hind limb than forelimb is among the distinctive characteristics of primate quadrupeds. Although often assumed to be due to a more posteriorly positioned whole body center of mass, there are little data to support such a difference. Reynolds (1985. Am J Phys Anthropol 67:335-349) notes that the distribution of forces on the limbs can also be influenced by average limb posture, but suggests that this effect is too small to account for the asymmetry in weight support observed in primates. Instead, he proposes that high hind limb forces are brought about by an active process of shifting weight off the forelimbs and onto the hind limbs through use of hind limb retractors. In this study, we use video records of walking animals to explore the degree to which average limb posture in primates and other quadrupedal mammals deviates from vertical, and use electromyography to test Reynolds' model of hind limb retractor activity and posterior weight shift. The limb posture results indicate that primate forelimbs oscillate about a vertical or slightly retracted axis, and though the hind limbs are slightly protracted, the magnitude of deviation from vertical is too small to have a major effect on weight support distribution. The electromyographic results reveal higher levels of hip extensor activity in antipronograde primates that bear a higher proportion of weight on their hind limbs. This lends support to Reynolds' suggestion that some primates use muscles to actively shift weight onto hind limbs to relieve stresses on forelimbs less well structured for weight support.     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

Apparent density patterns in subchondral bone of the sloth and anteater forelimb

Vertebrate morphologists often are interested in inferring limb-loading patterns in animals characterized by different locomotor repertoires. Because bone apparent density (i.e. mass per unit volume of bone inclusive of porosities) is a determinant of compressive strength, and thus indicative of compressive loading, recent comparative studies in primates have proposed a structure-function relationship between apparent density of subchondral bone and locomotor behaviours that vary in compressive loading. If such patterns are found in other mammals, then these relationships would be strengthened further. Here, we examine the distal radius of suspensory sloths that generally load their forelimbs (FLs) in tension and of quadrupedal anteaters that generally load their FLs in compression. Computed tomography osteoabsorptiometry was used to visualize the patterns in subchondral apparent density. Suspensory sloths exhibit relatively smaller areas of high apparent density than quadrupedal anteaters. This locomotor-based pattern is analogous to the pattern observed in suspensory and quadrupedal primates. Similarity between xenarthran and primate trends suggests broad-scale applicability for analysing subchondral bone apparent density and supports the idea that bone functionally alters its material properties in response to locomotor behaviours.     

Beneficial effect of hot spring bathing on stress levels in Japanese macaques

The ability of animals to survive dramatic climates depends on their physiology, morphology and behaviour, but is often influenced by the configuration of their habitat. Along with autonomic responses, thermoregulatory behaviours, including postural adjustments, social aggregation, and use of trees for shelter, help individuals maintain homeostasis across climate variations. Japanese macaques (Macaca fuscata) are the world’s most northerly species of nonhuman primates and have adapted to extremely cold environments. Given that thermoregulatory stress can increase glucocorticoid concentrations in primates, we hypothesized that by using an available hot spring, Japanese macaques could gain protection against weather-induced cold stress during winter. We studied 12 adult female Japanese macaques living in Jigokudani Monkey Park, Japan, during the spring birth season (April to June) and winter mating season (October to December). We collected faecal samples for determination of faecal glucocorticoid (fGC) metabolite concentrations by enzyme immunoassay, as well as behavioural data to determine time spent in the hot springs, dominance rank, aggression rates, and affiliative behaviours. We used nonparametric statistics to examine seasonal changes in hot spring bathing, and the relationship between rank and air temperature on hot spring bathing. We used general linear mixed-effect models to examine factors impacting hormone concentrations. We found that Japanese macaques use hot spring bathing for thermoregulation during the winter. In the studied troop, the single hot spring is a restricted resource favoured by dominant females. High social rank had both costs and benefits: dominant females sustained high fGC levels, which were associated with high aggression rates in winter, but benefited by priority of access to the hot spring, which was associated with low fGC concentrations and therefore might help reduce energy expenditure and subsequent body heat loss. This unique habit of hot spring bathing by Japanese macaques illustrates how behavioural flexibility can help counter cold climate stress, with likely implications for reproduction and survival.     

Positional Behavior of Black Spider Monkeys (Ateles paniscus) in French Guiana

Spider monkeys (Ateles) frequently use suspensory locomotion and postures, and their postcranial morphology suggests convergence with extant hominoids in canopy and food utilization. Previous studies of positional behavior in Ateles, have produced variable rates in the use of different positional activities. I investigated the positional behavior of black spider monkeys (Ateles paniscus) in a wet rain forest in French Guiana, and assessed differences in the rates of use of positional modes across studies. I also discuss the significance of suspensory activities in forest utilization. In French Guiana, Ateles confined travel and feeding locomotion on small and medium-sized moderately inclined supports in the main canopy. Tail-arm brachiation and clamber were their main traveling modes, while clamber was the dominant feeding locomotor mode. Small horizontal supports were predominant during their feeding. Suspensory postures accounted for more than half of feeding bouts, with tail-hang and tail-hind limb(s) hang being the dominant postures. Feeding occurred largely in tree crown peripheries with the prehensile tail anchored frequently above the monkey. They usually collected food items below or at the same level as the body. There is no difference among the postures they used to acquire and eat young leaves and fruit. My results agree with reports on the positional behavior of different species of spider monkeys at other sites. Despite the use of different methods, the same species exhibited more or less similar profiles in similar forests. Interspecific differences could be associated with morphological differences. Moreover, intraspecific differences could be attributed to forest structure. The findings suggest that the major part of biological information is independent of methods used in the several studies. Suspensory behavior facilitates the exploitation of the forest canopy by shortening traveling pathways between and within trees, by enabling faster travel for the better exploitation of patchy food sources and by providing access to food in the flexible terminal twigs.     

Involvement of the Chox-4 chicken homeobox genes in determination of anteroposterior axial polarity during limb development.

We have isolated and identified four chicken homeobox genes in the upstream region of the Chox-4 complex. The Chox-4g and -4f genes, at the 5' extremity of the complex, were expressed locally in the vicinity of the zone of polarizing activity (ZPA) at early stages of limb development, substantiating the involvement of the genes in anteroposterior axis determination. To confirm their function, we implanted a bead containing retinoic acid, or the ZPA itself, in the anterior margin of the limb bud, leading to formation of mirror-image duplicated digits, and observed the resultant change in gene expression. Expression of the Chox-4g and -4f genes was induced in the new digit-forming region. Those results suggest that positional information assigned by a ZPA morphogen is imprinted on cellular memory by expression of the Chox-4 genes to maintain positional signaling along the anteroposterior axis in the limb field.     

Perspectives on object manipulation and action grammar for percussive actions in primates

The skill of object manipulation is a common feature of primates including humans, although there are species-typical patterns of manipulation. Object manipulation can be used as a comparative scale of cognitive development, focusing on its complexity. Nut cracking in chimpanzees has the highest hierarchical complexity of tool use reported in non-human primates. An analysis of the patterns of object manipulation in naive chimpanzees after nut-cracking demonstrations revealed the cause of difficulties in learning nut-cracking behaviour. Various types of behaviours exhibited within a nut-cracking context can be examined in terms of the application of problem-solving strategies, focusing on their basis in causal understanding or insightful intentionality. Captive chimpanzees also exhibit complex forms of combinatory manipulation, which is the precursor of tool use. A new notation system of object manipulation was invented to assess grammatical rules in manipulative actions. The notation system of action grammar enabled direct comparisons to be made between primates including humans in a variety of object-manipulation tasks, including percussive-tool use.     

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

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