Intra-and interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool use

Tool manufacture and use have been described for wild orangutans (Pongo pygmaeus), with appreciable interpopulational differences in tool complexes. The ecological factors that contribute to these differences require investigation. Significant interpopulational differences in diet suggest that ecological factors contribute to variation in tool-based insect foraging. Using 4 years of behavioral data from the Suaq Balimbing Research Station (Sumatra, Indonesia), we tested predictions of two ecological hypotheses for the invention of tool use for insect foraging. We found limited evidence for inter- and intrasexual differences, as well as temporal variation, in activity budget and diet. However, differences did not correspond to variation in either rate of tool use or specialization on tool-based insectivory. Compared to other populations, orangutans at Suaq Balimbing ate significantly more insects. Low temporal variation in insectivory and an abundance of social insects at Suaq Balimbing suggest that insects formed a staple in the diet rather than a fallback food. Our findings do not support the hypothesis that tool use is a response to the low availability of primary food sources. Rather, greater opportunities for invention likely contributed to insect-extraction tool use at Suaq Balimbing.     

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. Am. J. Primatol. 74:1128‐1142, 2012. © 2012 Wiley Periodicals, Inc.     

Geographic variation in tool use on Neesia fruits in orangutans

Geographic variation in the presence of skilled behavior may reflect geographic variation in genetic predispositions or ecological conditions (accompanied by reliable expression during development), or it may reflect the vagaries of invention and the appropriate social conditions for persistence. In this study, we compare the feeding techniques and tool-using skills used by orangutans to extract the nutritious seeds from Neesia fruits between Suaq Balimbing on Sumatra and Gunung Palung on Borneo, and map the distribution of Neesia tool use in Sumatran swamps. We show that neither genetics nor ecology is sufficient to explain the distribution of this tool use, confirming earlier findings on chimpanzees. We conclude that the ability to learn to use tools determines the geographic distribution. It is impossible to distinguish between the history of invention and the conditions for social transmission as the causal factors, but the high density and the social tolerance at Suaq Balimbing create propitious conditions for the maintenance of the skill as a tradition once it has been invented. High orangutan densities in the other Sumatran coastal swamps with Neesia tool use support the conclusion that suitable transmission conditions are the critical factor to explain the geographic distribution of skills such as feeding tool use.     

Food Supply and Chimpanzee (Pan troglodytes schweinfurthii) Party Size in the Budongo Forest Reserve,Uganda

A central issue in socioecology is the nature of the relationship between an organism's environment and its social structure. In chimpanzees, the fission-fusion social system is thought to minimize feeding competition for primary dietary components: ephemeral, dispersed patches of ripe fruit. Intragroup feeding competition is thought to force individuals into small parties. Informal observations in the Sonso region of the Budongo forest had suggested that in this habitat, food supply was such that feeding competition was less important in determining grouping patterns than elsewhere. We used data collected on food supply and party sizes over a 4-year period to investigate this suggestion. In accord with theoretical expectation, sizes of foraging parties fluctuated with the size of food patches. However, party sizes showed either negative or no relationship with habitat-wide measures of food abundance. Likewise party sizes showed little relationship to overall measures of food dispersion. For important dietary items, both fruit and leaves had patchy distributions, though the degree of clumping was not strong, and fruit was not more clumped than leaves. Generally, abundant food appeared to be less patchy, and chimpanzees appeared to use more patches as food became more abundant rather than forming larger parties. We suggest that both dispersal and abundance need to be considered when investigating the impact of food supply on grouping patterns, and that the importance of food as a factor in determining chimpanzee grouping patterns declines with increasing levels of abundance.     

Individual variation in the rate of use of tree-hole tools among wild orang-utans: implications for hominin evolution

Primate tool use varies among species, populations, and individuals. Individual variation is especially poorly understood. Orang-utans in the Sumatran swamp forest of Suaq Balimbing varied widely in rates of tool use to extract honey, ants or termites from tree holes and in the degree to which they specialized on this tree-hole tool use. We tested whether individual variation was best explained by effects of social dominance, habitat differences, or by opportunities for socially learning the skills during ontogeny. There was no evidence for the first two hypotheses. However, we found a strong relationship between tool use specialization and mean female party size, which was used as a proxy for the opportunities for socially mediated learning in a foraging context during their development. This use was justified because females are rather philopatric and their mean party size remained stable over time, thus reflecting long-term tendencies. The correlation was not an artifact of a direct effect of party size on tool use tendencies, and did not hold for males, the dispersing sex. Thus, variation in the number of opportunities for social learning explains tool use variation within populations, corroborating hypotheses for between-population variation. The emergence of human culture was accompanied by vastly improved mechanisms of social learning. In order for these improvements to be favored by natural selection, the cultural potential must have actually been expressed. Thus, a combination of strong sociability and a reliance on tool-using or other technical skills acquired through social learning must have characterized early hominins.     

Group decision-making in fission-fusion societies

The prevalent view of group splitting during group decisions is that a beneficial consensus has not been reached because time constraints, different individual information, or inter-individual conflicts lead to fission instead of a compromise. However, societies with high fission-fusion dynamics may allow their members to avoid consensus decisions that are not in their favour without foregoing grouping benefits that arise from collective behaviour. Moreover, by forming temporary subgroups that represent individual preferences better than the group as a whole fission-fusion societies could avoid a permanent break up even in situations where conflicts among their members are to strong to reach a consensus.     

Behavioral Flexibility and the Evolution of Primate Social States

Comparative approaches to the evolution of primate social behavior have typically involved two distinct lines of inquiry. One has focused on phylogenetic analyses that treat social traits as static, species-specific characteristics; the other has focused on understanding the behavioral flexibility of particular populations or species in response to local ecological or demographic variables. Here, we combine these approaches by distinguishing between constraining traits such as dispersal regimes (male, female, or bi-sexual), which are relatively invariant, and responding traits such as grouping patterns (stable, fission-fusion, sometimes fission-fusion), which can reflect rapid adjustments to current conditions. Using long-term and cross-sectional data from 29 studies of 22 species of wild primates, we confirm that dispersal regime exhibits a strong phylogenetic signal in our sample. We then show that primate species with high variation in group size and adult sex ratios exhibit variability in grouping pattern (i.e., sometimes fission-fusion) with dispersal regime constraining the grouping response. When assessing demographic variation, we found a strong positive relationship between the variability in group size over time and the number of observation years, which further illustrates the importance of long-term demographic data to interpretations of social behavior. Our approach complements other comparative efforts to understand the role of behavioral flexibility by distinguishing between constraining and responding traits, and incorporating these distinctions into analyses of social states over evolutionary and ecological time.     

The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae)

A stable social group of 7 semifree-ranging black-and-white ruffed lemurs (Varecia variegata variegata) was studied for 4 months to catalog the behavioral repertoire of this species. Observations focussed on particular aspects of behavior were conducted before and after this 4-month period to supplement information gathered. Behavior in 11 major categories is detailed: postures, terrestrial locomotion, arboreal locomotion, feeding behavior, vocalizations, scent-marking, affinitive social behavior, agonistic social behavior, play behavior, sexual behavior, and parental behavior. Ruffed lemurs frequently used body positions and locomotor patterns unusual among lemurids, including bipedal hanging and long-descent leaps. These behaviors reinforce dental evidence that Varecia are among the most frugivorous of the Malagasy lemurs. Low intragroup cohesion, infrequent social interaction, and antiphonal use of several long-distance vocalizations suggest that ruffed lemurs naturally exhibit fission-fusion sociality. Social structure based on interindividual familiarity probably extends across foraging parties for several of the diurnally active lemurs; however, thus far only Varecia seems likely to exhibit fission-fusion sociality analogous to that seen in spider monkeys and chimpanzees.     

Mahale chimpanzees: grouping patterns and cycling females

The social system of chimpanzees (Pan troglodytes schweinfurthii) is characterized by the fission-fusion of social groups. Several studies have reported that females are less gregarious than males. In the current study, adult female gregariousness depended on their reproductive state. Noncycling adult females (pregnant, lactating, or post reproductive) were observed in large bisexual parties less often than cycling adult females. On the other hand, cycling adult females were observed in large bisexual parties as often as males, regardless of their estrous state. More males were in parties that included cycling adult females with maximal genital swelling (estrous females) than in parties without them. Moreover, a bisexual party including more estrous females contained more males. These results suggest that large bisexual parties of chimpanzees are constructed by a dual mechanism. First, cycling adult females are attracted to parties that consist of the top ranking male and large numbers of adult and adolescent males. Second, adult and adolescent males that did not belong to parties originally are attracted by estrous females and join them. Thus, in Mahale Mountains National Park, Tanzania, bisexual parties of chimpanzees can be characterized as "parties for reproduction."     

From individuals to aggregations: the interplay between behavior and physics

This paper analyses the processes by which organisms form groups and how social forces interact with environmental variability and transport. For aquatic organisms, the latter is especially important-will sheared or turbulent flows disrupt organism groups? To analyse such problems, we use individual-based models to study the environmental and social forces leading to grouping. The models are then embedded in turbulent flow fields to gain an understanding of the interplay between the forces acting on the individuals and the transport induced by the fluid motion. Instead of disruption of groups, we find that flows often enhance grouping by increasing the encounter rate among groups and thereby promoting merger into larger groups; the effect breaks down for strong flows. We discuss the transformation of individual-based models into continuum models for the density of organisms. A number of subtle difficulties arise in this process; however, we find that a direct comparison between the individual model and the continuum model is quite favorable. Finally, we examine the dynamics of group statistics and give an example of building an equation for the spatial and temporal variations of the group-size distribution from the individual-based simulations. These studies lay the groundwork for incorporating the effects of grouping into models of the large scale distributions of organisms as well as for examining the evolutionary consequences of group formation.     

Social organization of savanna-dwelling chimpanzees,Pan troglodytes verus,at Mt. Assirik,Senegal

A community of chimpanzees at Mt. Assirik in south-eastern Senegal subsists in a hot, dry and open environment. This wide-ranging, savanna-living group provides an opportunity for comparisons of social organization with other population elsewhere in Africa living in forest and woodland. The group numbered about 28 over the four-year study, and its composition by age and sex was typical. The average size of parties (i.e., temporary sub-groups) did not differ from other populations. However, a high proportion of the group tended to remain together in such parties. The composition of parties resembled that found elsewhere, but some differences emerged between the wet and dry seasons. Larger, mixed parties containing adult males were much more common in open, non-forested habitats than were solitary individuals or parties without adult males. Large parties tended to form for travelling, especially for rapid movement over long distances. Such aspects of social organization seem unlikely to be related to the availability of food in any simple way. Instead, they seem to be adaptations to threat from predators and patchily distributed food, water and nesting sites. This results in occasional bivouacs and mass-migrations from one part of the home-range to another, especially in the dry season.     

Factors affecting party size and composition of chimpanzees (Pan troglodytes verus) Bossou,Guinea

I studied the party sizes of western chimpanzees (Pan troglodytes verus)and factors assumed to affect them at Bossou, Republic of Guinea, West Africa. Party size is negatively correlated with feeding ratio, and larger parties tend to be formed in more dangerous situations (i.e. crossing roads with much traffic). When parties included estrous females, young (i.e., late juvenile and adolescent) males tended to forage with them, independently from their mothers. Lactating females with infants tended to spend more time alone, but the trend was not as apparent as it is in P. t. schweinfurthiat Gombe, Tanzania. These facts suggest that several factors, in addition to food availability, affect party formation, or fission-fusion, of chimpanzees. I also briefly discuss comparatively the pattern of party formation in P. paniscus.     

Embraces and Grooming in Captive Spider Monkeys

Relatively little information is available regarding the role of social grooming and embraces in spider monkeys that live in fission-fusion societies in which individuals are usually split into subgroups. We investigated whether embraces and grooming have similar roles in captive spider monkeys by examining their occurrence in two contexts. One context was fusion, i.e. when the monkeys moved into an area of the enclosure where other monkeys were present, in which individuals from different subgroups were expected to exchange greeting behavior. The other context was the access to young infants, in which females were expected increase their friendly behavior toward mothers. We collected data by observing all individuals within a subgroup and via focal animal sampling. We found that overall embraces occurred more frequently than grooming and that their distributions were not correlated. The frequency of embraces was positively associated with the number of fusion events per observation, whereas the frequency of grooming bouts was not. Furthermore, embraces were more frequent following initial approaches after fusion versus subsequent approaches, and the figure was higher than the corresponding one for grooming. Mothers received more embraces after than before the birth of their infants, whereas there was no such effect for grooming. Embraces, but not grooming, play a role in the regulation of social relationships in spider monkeys. Embraces may serve as signals of benign disposition in contexts that are likely to be associated with tension, such as fusion and access to infants.     

The Evolution of Different Forms of Sociality: Behavioral Mechanisms and Eco-Evolutionary Feedback

Different forms of sociality have evolved via unique evolutionary trajectories. However, it remains unknown to what extent trajectories of social evolution depend on the specific characteristics of different species. Our approach to studying such trajectories is to use evolutionary case-studies, so that we can investigate how grouping co-evolves with a multitude of individual characteristics. Here we focus on anti-predator vigilance and foraging. We use an individual-based model, where behavioral mechanisms are specified, and costs and benefits are not predefined. We show that evolutionary changes in grouping alter selection pressures on vigilance, and vice versa. This eco-evolutionary feedback generates an evolutionary progression from “leader-follower” societies to “fission-fusion” societies, where cooperative vigilance in groups is maintained via a balance between within- and between-group selection. Group-level selection is generated from an assortment that arises spontaneously when vigilant and non-vigilant foragers have different grouping tendencies. The evolutionary maintenance of small groups, and cooperative vigilance in those groups, is therefore achieved simultaneously. The evolutionary phases, and the transitions between them, depend strongly on behavioral mechanisms. Thus, integrating behavioral mechanisms and eco-evolutionary feedback is critical for understanding what kinds of intermediate stages are involved during the evolution of particular forms of sociality.     

The development of wild immature Sumatran orangutans (Pongo abelii) at Ketambe

Orangutans have the longest immature period and inter-birth interval of all ape species. This may be explained by a slow life history, the need to develop skills or by their relatively solitary lifestyle, which prevents a mother from associating with two offspring. This study of wild immature orangutans at the Ketambe Research Station, Indonesia, describes, with partly cross-sectional, partly longitudinal data, their development to independence. The study subjects ranged from 1 to 11 years of age. Data on their activity budget, diet, mother–offspring proximity and maintenance of proximity, association with conspecifics and play behavior were collected. The results indicate that immature orangutans can provide for their own food and transport, and therefore were independent of direct maternal care, at an age of possibly 3 but more clearly 6 years. This is similar to chimpanzees, and refutes the slow life history hypothesis. Immature orangutans remain within their mother’s vicinity until the age of 8 years, indicating a dependence on indirect maternal care, and this coincides with the period during which the mother does not produce another offspring. A female orangutan seems unable to associate with an older immature while caring for a new infant. This is consistent with the solitary-lifestyle hypothesis and corroborates the results obtained with the Sumatran orangutan population at Suaq Balimbing. However, why an immature depends indirectly on its mother for such a long period remains unclear. It is possible that it needs to develop ecological or social skills or needs the protection of its mother. Unfortunately, no data were available to distinguish between these possibilities.     

Party composition and dynamics inPan paniscus

The pygmy chimpanzee, or bonobo, Pan paniscus,diplays a fission-fusion social organization in which individuals associate in parties that vary in size and composition. Data from a 2-year field study of nonprovisioned P. paniscusshow that party composition varies with party size. Although females, on average, outnumber males, the proportion of males in the party increases in larger parties. This effect was not due to the greater number of known females. Both females and males will join and leave a party in the company of others, but only males appear frequently to join or leave as lone individuals. All-male parties were not observed, but all-female (nonnursery) parties were relatively common. These trends reflect greater cohesion among females than observed in P. troglodytes schweinfurthii.Cohesion between males and female P. paniscusmay increase with party size.     

Fission–fusion social systems as a strategy for coping with ecological constraints: a primate case

Fission–fusion social systems, in which members of a social community form frequently changing subgroups, occur in a number of mammalian taxa. Such systems are assumed to be a response to the costs of grouping, but evidence to support this hypothesis is limited. We use a linear programming approach to build a time budget model that predicts the upper bound on group size in order to test the hypothesis that fission–fusion social systems are the outcome of time constraints. Comparative data from 14 wild chimpanzee (Pan spp.) populations are used to derive a set of equations defining the relationship between climatic variables and time budget components, which are then used to calculate the upper limits on group size that can be maintained in different habitats. We validate the model by showing that it correctly predicts the presence/absence of chimpanzees across sub-Saharan Africa and the group sizes observed in natural populations. The model suggests that the costs of travel are limiting for chimpanzees. Chimpanzees can reduce these costs dramatically by fissioning their bonded communities into small foraging parties. If they did not, they would be unable to live in any habitats where they currently occur.     

Demography,ranging patterns,and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park,Peru

Results of a long-term field study on the ecology and social organization of two groups of black spider monkeys (Ateles paniscus chamek) in Peru are reported. Demography, ranging patterns, and activity budgets provide insight into some of the proximate determinants of fission-fusion social organization in this species and illustrate the different strategies used by males and females to gain access to critical resources. Longitudinal data on known individuals provide evidence for male natal philopatry and female emigration at sexual maturity in this population. Interbirth intervals are long (mean = 34.5 months) in comparison with most other primate species, and 5 of 15 infants seen within a few days of birth died or disappeared before they were a year old. Home ranges are large (150–250 ha) and fairly discrete; overlap with neighboring groups is on the order of 10–15%. Males and females differed substantially in their ranging patterns; females, particularly those with infants, restricted much of their ranging to a “core area” 20–33% the size of the total group range, whereas males ranged more evenly over the entire area occupied by the group. Daily path length varied over almost an order of magnitude from 465 m to 4,070 m, with a mean of 1977 m. Males spent more time traveling and less time feeding than most females. These results are compared with those obtained in previous studies of Ateles and with similar data from other primate species to assess their implications for the evolution of fission-fusion sociality in spider monkeys. The ecological factors responsible for the evolution of very similar social organizations in spider monkeys and chimpanzees are discussed.     

Aggression and conflict management at fusion in spider monkeys

In social systems characterized by a high degree of fission-fusion dynamics, members of a large community are rarely all together, spending most of their time in smaller subgroups with flexible membership. Although fissioning into smaller subgroups is believed to reduce conflict among community members, fusions may create conflict among individuals from joining subgroups. Here, we present evidence for aggressive escalation at fusion and its mitigation by the use of embraces in wild spider monkeys (Ateles geoffroyi). Our findings provide the first systematic evidence for conflict management at fusion and may have implications for the function of human greetings.