The role of great ape behavioral ecology in One Health: Implications for captive welfare and re-habilitation success.

Behavior is the interface through which animals interact with their environments, and therefore has potentially cascading impacts on the health of individuals, populations, their habitats, and the humans that share them. Evolution has shaped the interaction between species and their environments. Thus, alterations to the species-typical "wild-type" behavioral repertoire (and the ability of the individual to adapt flexibly which elements of the repertoire it employs) may disrupt the relationship between the organism and its environment, creating cascading One Health effects. A good example is rehabilitant orangutans where, for example, seemingly minor differences from wild conspecifics in the time spent traveling on the ground rather than in the forest canopy can affect an individual's musculoskeletal and nutritional health, as well as social integration. It can also increase two-way transmission of infectious diseases and/or pathogens with local human populations, or potentially with neighboring wild populations if there are no geographical barriers and rehabilitants travel far enough to leave their release area. Primates are well known ecosystem engineers, reshaping plant communities and maintaining biodiversity through seed dispersal, consuming plants, and creating canopy gaps and trails. From the habitat perspective, a rehabilitant orangutan which does not behave like a wild orangutan is unlikely to fulfill these same ecosystem services. Despite the importance of the diversity of an ape's behavioral repertoire, how it compares to that of wild conspecifics and how it alters in response to habitat variation, behavior is an often under-appreciated aspect of One Health. In this review, focusing on orangutans as an example of the kinds of problems faced by all captive great apes, we examine the ways in which understanding and facilitating the expression of wild-type behavior can improve their health, their ability to thrive, and the robustness of local One Health systems.

Practice makes perfect: Performance optimisation in 'arboreal' parkour athletes illuminates the evolutionary ecology of great ape anatomy.

An animal's size is central to its ecology, yet remarkably little is known about the selective pressures that drive this trait. A particularly compelling example is how ancestral apes evolved large body mass in such a physically and energetically challenging environment as the forest canopy, where weight-bearing branches and lianas are flexible, irregular and discontinuous, and the majority of preferred foods are situated on the most flexible branches at the periphery of tree crowns. To date the issue has been intractable due to a lack of relevant fossil material, the limited capacity of the fossil record to reconstruct an animal's behavioural ecology and the inability to measure energy consumption in freely moving apes. We studied the oxygen consumption of parkour athletes while they traversed an arboreal-like course as an elite model ape, to test the ecomorphological and behavioural mechanisms by which a large-bodied ape could optimize its energetic performance during tree-based locomotion. Our results show that familiarity with the arboreal-like course allowed the athletes to substantially reduce their energy expenditure. Furthermore, athletes with larger arm spans and shorter legs were particularly adept at finding energetic savings. Our results flesh out the scanty fossil record to offer evidence that long, strong arms, broad chests and a strong axial system, combined with the frequent use of uniform branch-to-branch arboreal pathways, were critical to off-setting the mechanical and energetic demands of large mass in ancestral apes.

Bridging the gap: parkour athletes provide new insights into locomotion energetics of arboreal apes.

The tree canopy is an energetically challenging environment to traverse. Along with compliant vegetation, gaps in the canopy can prove energetically costly if they force a route-extending detour. Arboreal apes exhibit diverse locomotion strategies, including for gap crossing. Which one they employ in any given scenario may be influenced by the energy costs to do so, which are affected by the details of the immediate environment in combination with their body size. Measuring energetics of arboreal apes is not tractable; thus our knowledge in this area is limited. We devised a novel, custom-made experimental set-up to record the energy expenditure of parkour athletes tree-swaying, jumping and vertical climbing. The latter strategy was vastly more expensive, indicating that when energy economy is the focus arboreal apes will prioritize routes that limit height changes. Whether tree-swaying or jumping was most economical for the athletes depended upon interactions between tree stiffness, the distance to cross, number of tree-sways required and their own mass. Updated analysis of previous interspecific correlations suggests that whether the relative costs to vertical climb are size-invariant across primate species is complicated by details of the climbing context.

Nest-building orangutans demonstrate engineering know-how to produce safe, comfortable beds.

Nest-building orangutans must daily build safe and comfortable nest structures in the forest canopy and do this quickly and effectively using the branches that surround them. This study aimed to investigate the mechanical design and architecture of orangutan nests and determine the degree of technical sophistication used in their construction. We measured the whole nest compliance and the thickness of the branches used and recorded the ways in which the branches were fractured. Branch samples were also collected from the nests and subjected to three-point bending tests to determine their mechanical properties. We demonstrated that the center of the nest is more compliant than the edges; this may add extra comfort and safety to the structure. During construction orangutans use the fact that branches only break half-way across in "greenstick" fracture to weave the main nest structure. They choose thicker branches with greater rigidity and strength to build the main structure in this way. They then detach thinner branches by following greenstick fracture with a twisting action to make the lining. These results suggest that orangutans exhibit a degree of technical knowledge and choice in the construction of nests.

Development of planning in 4- to 10-year-old children: reducing inhibitory demands does not improve performance.

Currently, there are relatively few tasks suitable for testing planned problem solving in children. We presented 4- to 10-year-old children (N=172) with two planning tasks (sequential planning and advance planning) using the paddle-box apparatus, which was originally designed to investigate the planning skills of nonhuman apes. First, we were interested in the development of children's performance in the two tasks and whether the strategies children used to succeed differed among age groups. Performance improved significantly across age groups in both tasks. Strategies for success in the advance planning task differed among age groups, with 4- and 5-year-olds performing more excess actions, and a greater proportion of irrelevant excess actions, than older children. Findings are discussed in relation to the development of performance in tower tasks, which are a commonly used test of planning ability in humans. Second, based on previous findings with apes, we predicted that introducing measures to reduce the inhibitory demands of the advance planning task would improve children's performance. Therefore, in this study we introduced two methodological alterations that have been shown to improve children's performance in other tasks with inhibitory demands: (a) imposing a short delay before a child is allowed to act and (b) replacing reward items with symbolic tokens. Surprisingly, neither of these measures improved the performance of children in any of the age groups, suggesting that, contrary to our prediction, inhibitory control might not be a key performance-limiting factor in the advance planning paddle-box task.

Functional adaptations in the forelimb muscles of non-human great apes.

The maximum capability of a muscle can be estimated from simple measurements of muscle architecture such as muscle belly mass, fascicle length and physiological cross-sectional area. While the hindlimb anatomy of the non-human apes has been studied in some detail, a comparative study of the forelimb architecture across a number of species has never been undertaken. Here we present data from chimpanzees, bonobos, gorillas and an orangutan to ascertain if, and where, there are functional differences relating to their different locomotor repertoires and habitat usage. We employed a combination of analyses including allometric scaling and ancovas to explore the data, as the sample size was relatively small and heterogeneous (specimens of different sizes, ages and sex). Overall, subject to possible unidentified, confounding factors such as age effects, it appears that the non-human great apes in this sample (the largest assembled to date) do not vary greatly across different muscle architecture parameters, even though they perform different locomotor behaviours at different frequencies. Therefore, it currently appears that the time spent performing a particular behaviour does not necessarily impose a dominating selective influence on the soft-tissue portion of the musculoskeletal system; rather, the overall consistency of muscle architectural properties both between and within the Asian and African apes strengthens the case for the hypothesis of a possible ancient shared evolutionary origin for orthogrady under compressive and/or suspensory loading in the great apes.

What cognitive strategies do orangutans (Pongo pygmaeus) use to solve a trial-unique puzzle-tube task incorporating multiple obstacles?

Apparently sophisticated behaviour during problem-solving is often the product of simple underlying mechanisms, such as associative learning or the use of procedural rules. These and other more parsimonious explanations need to be eliminated before higher-level cognitive processes such as causal reasoning or planning can be inferred. We presented three Bornean orangutans with 64 trial-unique configurations of a puzzle-tube to investigate whether they were able to consider multiple obstacles in two alternative paths, and subsequently choose the correct direction in which to move a reward in order to retrieve it. We were particularly interested in how subjects attempted to solve the task, namely which behavioural strategies they could have been using, as this is how we may begin to elucidate the cognitive mechanisms underpinning their choices. To explore this, we simulated performance outcomes across the 64 trials for various procedural rules and rule combinations that subjects may have been using based on the configuration of different obstacles. Two of the three subjects solved the task, suggesting that they were able to consider at least some of the obstacles in the puzzle-tube before executing action to retrieve the reward. This is impressive compared with the past performances of great apes on similar, arguably less complex tasks. Successful subjects may have been using a heuristic rule combination based on what they deemed to be the most relevant cue (the configuration of the puzzle-tube ends), which may be a cognitively economical strategy.

Forest structure and support availability influence orangutan locomotion in Sumatra and Borneo.

The influence of habitat structure and support availability on support use is an important aspect of understanding locomotor behavior in arboreal primates. We compared habitat structure and support availability in three orangutan study sites-two on Sumatra (Pongo abelii) in the dry-lowland forest of Ketambe and peat swamp forest of Suaq Balimbing, and one on Borneo (Pongo pygmaeus wurmbii) in the disturbed peat swamp forest of Sabangau-to better understand orangutan habitat use. Our analysis revealed vast differences in tree and liana density between the three sites. Sabangau had a much higher overall tree density, although both Sumatran sites had a higher density of larger trees. The two peat swamp forests were more similar to each other than to Ketambe, particularly with regard to support availability. Ketambe had a wider variety of supports of different sizes and types, and a higher density of larger lianas than the two peat swamps. Orangutans in all three sites did not differ substantially in terms of their preferred supports, although Sumatran orangutans had a strong tendency to use lianas, not observed in Sabangau. Differences in observed frequencies of locomotor behavior suggest the homogeneous structure of Sabangau limits the locomotor repertoire of orangutans, with high frequencies of fewer behaviors, whereas the wider range of supports in Ketambe appears to have facilitated a more varied locomotor repertoire. There were no differences among age-sex classes in the use of arboreal pathways in Suaq Balimbing, where orangutans selected larger trees than were typically available. This was less apparent in Sabangau, where orangutans generally used trees in relation to their environmental abundance, reflecting the homogeneous nature of disturbed peat swamp forest. These results demonstrate that forest architecture has an important influence on orangutan locomotion, which may become increasingly important as the structure of orangutan habitat continues to be altered through human disturbance.

Orangutans employ unique strategies to control branch flexibility.

Orangutans are the largest habitually arboreal mammal. For them, as for all arboreal mammals, access to the abundant fruits and narrowest gaps found among the thin peripheral branches of tree crowns poses considerable safety risks and energetic demands. Most arboreal primates use flexed-limb postures to minimize problems caused by branch compliance and instability. Here, we show that Sumatran orangutans employ unique locomotor strategies to control compliance and allow access to the terminal branch niche for feeding and gap crossing. We calculated a "stiffness score," which is a measure of the flexibility of the supports on which orangutans moved. We found that certain locomotor behaviors clearly are associated with the most compliant supports; these behaviors appear to lack regular limb sequences, which serves to avoid the risk of resonance in branch sway caused by high-frequency, patterned gait. Balance and increased stability are achieved through long contact times between multiple limbs and supports and a combination of pronograde (horizontal) and orthograde (vertical) body postures, used both above branches and in suspension underneath them. Overall, adult females seem to be the most conservative in their travel, selecting more solid and secure supports than males and adolescents. These results have implications for understanding locomotor diversity in fossil and extant apes and for orangutan conservation and reintroduction programs.

Distribution patterns of fibre types in the triceps surae muscle group of chimpanzees and orangutans.

Different locomotor and postural demands are met partly due to the varying properties and proportions of the muscle fibre types within the skeletal muscles. Such data are therefore important in understanding the subtle relationships between morphology, function and behaviour. The triceps surae muscle group is of particular interest when studying our closest living relatives, the non-human great apes, as they lack a significant external Achilles tendon, crucial to running locomotion in humans and other cursorial species. The aim of this study, therefore, was to determine the proportions of type I (slow) and type II (fast) fibres throughout these muscles in chimpanzees and orangutans using immunohistochemistry. The orangutan had a higher proportion of type I fibres in all muscles compared with the chimpanzees, related to their slower, more controlled movements in their arboreal habitat. The higher proportion of type II fibres in the chimpanzees likely reflects a compromise between their need for controlled mobility when arboreal, and greater speed and power when terrestrial. Overall, the proportion of slow fibres was greater in the soleus muscle compared with the gastrocnemius muscles, and there was some evidence of proximal to distal and medial to lateral variations within some muscles. This study has shown that not only do orangutans and chimpanzees have very different muscle fibre populations that reflect their locomotor repertoires, but it also shows how the proportion of fibre types provides an additional mechanism by which the performance of a muscle can be modulated to suit the needs of a species.

Hindlimb muscle architecture in non-human great apes and a comparison of methods for analysing inter-species variation.

By relating an animal's morphology to its functional role and the behaviours performed, we can further develop our understanding of the selective factors and constraints acting on the adaptations of great apes. Comparison of muscle architecture between different ape species, however, is difficult because only small sample sizes are ever available. Further, such samples are often comprised of different age-sex classes, so studies have to rely on scaling techniques to remove body mass differences. However, the reliability of such scaling techniques has been questioned. As datasets increase in size, more reliable statistical analysis may eventually become possible. Here we employ geometric and allometric scaling techniques, and ancovas (a form of general linear model, GLM) to highlight and explore the different methods available for comparing functional morphology in the non-human great apes. Our results underline the importance of regressing data against a suitable body size variable to ascertain the relationship (geometric or allometric) and of choosing appropriate exponents by which to scale data. ancova models, while likely to be more robust than scaling for species comparisons when sample sizes are high, suffer from reduced power when sample sizes are low. Therefore, until sample sizes are radically increased it is preferable to include scaling analyses along with ancovas in data exploration. Overall, the results obtained from the different methods show little significant variation, whether in muscle belly mass, fascicle length or physiological cross-sectional area between the different species. This may reflect relatively close evolutionary relationships of the non-human great apes; a universal influence on morphology of generalised orthograde locomotor behaviours or, quite likely, both.

Locomotor behavior of wild orangutans (Pongo pygmaeus wurmbii) in disturbed peat swamp forest, Sabangau, Central Kalimantan, Indonesia.

This study examined the locomotor behavior of wild Bornean orangutans (P. p. wurmbii) in an area of disturbed peat swamp forest (Sabangau Catchment, Indonesia) in relation to the height in the canopy, age-sex class, behavior (feeding or traveling), and the number of supports used to bear body mass. Backward elimination log-linear modeling was employed to expose the main influences on orangutan locomotion. Our results showed that the most important distinctions with regard to locomotion were between suspensory and compressive, or, orthograde (vertical trunk) and pronograde (horizontal trunk) behavior. Whether orangutans were traveling or feeding had the most important influence on locomotion whereby compressive locomotion had a strong association with feeding, suspensory locomotion had a strong association with travel in the peripheral strata using multiple supports, whereas vertical climb/descent and oscillation showed a strong association with travel on single supports in the core stratum. In contrast to theoretical predictions on positional behavior and body size, age-sex category had a limited influence on locomotion. The study revealed that torso orthograde suspension dominates orangutan locomotion, concurring with previous studies in dipterocarp forest. But, orangutans in the Sabangau exhibited substantially higher frequencies of oscillatory locomotion than observed at other sites, suggesting this behavior confers particular benefits for traversing the highly compliant arboreal environment typical of disturbed peat swamp forest. In addition, torso pronograde suspensory locomotion was observed at much lower levels than in the Sumatran species. Together these results highlight the necessity for further examination of differences between species, which control for habitat.

The Ontogeny of Gap Crossing Behaviour in Bornean Orangutans (Pongo pygmaeus wurmbii).

For orangutans, the largest predominantly arboreal primates, discontinuous canopy presents a particular challenge. The shortest gaps between trees lie between thin peripheral branches, which offer the least stability to large animals. The affordances of the forest canopy experienced by orangutans of different ages however, must vary substantially as adult males are an order of magnitude larger in size than infants during the early stages of locomotor independence. Orangutans have developed a diverse range of locomotor behaviour to cross gaps between trees, which vary in their physical and cognitive demands. The aims of this study were to examine the ontogeny of orangutan gap crossing behaviours and to determine which factors influence the distance orangutans crossed. A non-invasive photographic technique was used to quantify forearm length as a measure of body size. We also recorded locomotor behaviour, support use and the distance crossed between trees. Our results suggest that gap crossing varies with both physical and cognitive development. More complex locomotor behaviours, which utilized compliant trunks and lianas, were used to cross the largest gaps, but these peaked in frequency much earlier than expected, between the ages of 4 and 5 years old, which probably reflects play behaviour to perfect locomotor techniques. Smaller individuals also crossed disproportionately large gaps relative to their size, by using support deformation. Our results suggest that orangutans acquire the full repertoire of gap crossing techniques, including the more cognitively demanding ones, before weaning, but adjust the frequency of the use of these techniques to their increasing body size.

Does perceived steepness deter stair climbing when an alternative is available?

Perception of hill slant is exaggerated in explicit awareness. Proffitt (Perspectives on Psychological Science 1:110-122, 2006) argued that explicit perception of the slant of a climb allows individuals to plan locomotion in keeping with their available locomotor resources, yet no behavioral evidence supports this contention. Pedestrians in a built environment can often avoid climbing stairs, the man-made equivalent of steep hills, by choosing an adjacent escalator. Stair climbing is avoided more by women, the old, and the overweight than by their comparators. Two studies tested perceived steepness of the stairs as a cue that promotes this avoidance. In the first study, participants estimated the steepness of a staircase in a train station (n = 269). Sex, age, height, and weight were recorded. Women, older individuals, and those who were heavier and shorter reported the staircase as steeper than did their comparison groups. In a follow-up study in a shopping mall, pedestrians were recruited from those who chose the stairs and those who avoided them, with the samples stratified for sex, age, and weight status. Participants (n = 229) estimated the steepness of a life-sized image of the stairs they had just encountered, presented on the wall of a vacant shop in the mall. Pedestrians who avoided stair climbing by choosing the escalator reported the stairs as steeper even when demographic differences were controlled. Perceived steepness may to be a contextual cue that pedestrians use to avoid stair climbing when an alternative is available.

A novel test of planning ability: great apes can plan step-by-step but not in advance of action.

The ability to identify an appropriate sequence of actions or to consider alternative possible action sequences might be particularly useful during problem solving in the physical domain. We developed a new 'paddle-box' task to test the ability of different ape species to plan an appropriate sequence of physical actions (rotating paddles) to retrieve a reward from a goal location. The task had an adjustable difficulty level and was not dependent on species-specific behaviours (e.g. complex tool use). We investigated the planning abilities of captive orangutans (Pongo pygmaeus) and bonobos (Pan paniscus) using the paddle-box. In experiment 1, subjects had to rotate one or two paddles before rotating the paddle with the reward on. Subjects of both species performed poorly, though orangutans rotated more non-food paddles, which may be related to their greater exploratory tendencies and bolder temperament compared with bonobos. In experiment 2 subjects could always rotate the paddle with the reward on first and still succeed, and most subjects of both species performed appropriate sequences of up to three paddle rotations to retrieve the reward. Poor performance in experiment 1 may have been related to subjects' difficulty in inhibiting the prepotent response to act on the reward immediately.

Factors affecting the compliance and sway properties of tree branches used by the Sumatran orangutan (Pongo abelii).

The tropical arboreal environment is a mechanically complex and varied habitat. Arboreal inhabitants must adapt to changes in the compliance and stability of supports when moving around trees. Because the orangutan is the largest habitual arboreal inhabitant, it is unusually susceptible to branch compliance and stability and therefore represents a unique animal model to help investigate how animals cope with the mechanical heterogeneity of the tropical canopy. The aim of this study was to investigate how changes in compliance and time of oscillation of branches are related to easily observable traits of arboreal supports. This should help predict how supports react mechanically to the weight and mass of a moving orangutan, and suggest how orangutans themselves predict branch properties. We measured the compliance and time of oscillation of branches from 11 tree species frequented by orangutans in the rainforest of Sumatra. Branches were pulled at several points along their length using a force balance at the end of a stiff rope, and the local diameter of the branch and the distance to its base and tip were measured. Compliance was negatively associated with both local diameter and length to the tip of the branch, and positively, if weakly, associated with length from the trunk. However, branch diameter not only predicted compliance best, but would also be easiest for an orangutan to observe. In contrast, oscillation times of branches were largely unaffected by local diameter, and only significantly increased at diameters below 2 cm. The results of this study validate previous field research, which related locomotory modes to local branch diameter, while suggesting how arboreal animals themselves sense their mechanical environment.

Arboreality, terrestriality and bipedalism.

The full publication of Ardipithecus ramidus has particular importance for the origins of hominin bipedality, and strengthens the growing case for an arboreal origin. Palaeontological techniques however inevitably concentrate on details of fragmentary postcranial bones and can benefit from a whole-animal perspective. This can be provided by field studies of locomotor behaviour, which provide a real-world perspective of adaptive context, against which conclusions drawn from palaeontology and comparative osteology may be assessed and honed. Increasingly sophisticated dynamic modelling techniques, validated against experimental data for living animals, offer a different perspective where evolutionary and virtual ablation experiments, impossible for living mammals, may be run in silico, and these can analyse not only the interactions and behaviour of rigid segments but increasingly the effects of compliance, which are of crucial importance in guiding the evolution of an arboreally derived lineage.

Testing the use/disuse hypothesis: pectoral and leg muscle changes in captive barnacle geese Branta leucopsis during wing moult.

Previous studies on wild moulting waterfowl have demonstrated that flight and leg muscles experience periods of hypertrophy and atrophy. This is thought to be in response to the change in use of the locomotor muscles as described in the use/disuse hypothesis. We tested this hypothesis using captive barnacle geese. Forty geese were dissected before, during and after wing moult, to determine the changes in mass and functional capacity of the flight and leg muscles. Physiological cross sectional areas (PCSA) and mean fascicle lengths of functional muscle groups were calculated to ascertain the force-producing capabilities of the flight and leg muscles. At the onset of moult, flight muscle mass was at a minimum, having atrophied by 35% compared with pre-moult levels, but it returned to pre-moult levels by the end of wing moult. By contrast, the leg muscles hypertrophied during wing moult by 29%, and the PCSA of individual muscle groups increased substantially. Increases in mass, PCSA and fascicle length of individual leg muscle groups during moult suggest that, when flightless, the leg muscles are functionally adapted to provide greater force and/or manoeuvrability to the birds, to aid ground-based escape from predators. Through studying captive animals that are unable to fly, it has been possible to conclude that the major changes in leg and flight muscle in moulting captive geese cannot be explained through use or disuse. Instead, changes seem to be compensatory or to occur in anticipation of changes in locomotor patterns.

Orangutan positional behavior and the nature of arboreal locomotion in Hominoidea.

The Asian apes, more than any other, are restricted to an arboreal habitat. They are consequently an important model in the interpretation of the morphological commonalities of the apes, which are locomotor features associated with arboreal living. This paper presents a detailed analysis of orangutan positional behavior for all age-sex categories and during a complete range of behavioral contexts, following standardized positional mode descriptions proposed by Hunt et al. ([1996] Primates 37:363-387). This paper shows that orangutan positional behavior is highly complex, representing a diverse spectrum of positional modes. Overall, all orthograde and pronograde suspensory postures are exhibited less frequently in the present study than previously reported. Orthograde suspensory locomotion is also exhibited less often, whereas pronograde and orthograde compressive locomotor modes are observed more frequently. Given the complexity of orangutan positional behavior demonstrated by this study, it is likely that differences in positional behavior between studies reflect differences in the interplay between the complex array of variables, which were shown to influence orangutan positional behavior (Thorpe and Crompton 2005 Am. J. Phys. Anthropol. 127:58-78). With the exception of pronograde suspensory posture and locomotion, orangutan positional behavior is similar to that of the African apes, and in particular, lowland gorillas. This study suggests that it is orthogrady in general, rather than forelimb suspend specifically, that characterizes the positional behavior of hominoids.