Chimpanzee Communities Research Articles

Male chimpanzees compromise the foraging success of their mates in Kibale National Park, Uganda

Sexual conflict develops when the optimal reproductive strategy for one sex inflicts fitness costs upon the other sex. Among species with intense within-group feeding competition and high costs of reproduction, females are expected to experience reduced foraging efficiency by associating with males, and this may compromise their reproductive ability. Here, we test this hypothesis in chimpanzees, a species with flexible grouping patterns in which female avoidance of large subgroups has been attributed to their relatively high costs of grouping. In an >11-year study of the Kanyawara community of East African chimpanzees (Pan troglodytes schweinfurthii) in the Kibale National Park, Uganda, the availability of sexually receptive females was a key determinant of the number of males in parties. In turn, females experienced significantly lower C-peptide of insulin levels, indicative of reduced energy balance, during periods when they associated with more males. Female associates did not produce the same negative effect. C-peptide levels positively and significantly predicted female ovarian steroid production, indicating that the costs of associating with males can lead to downstream reproductive costs. Therefore, we conclude that Kanyawara chimpanzees exhibit sexual conflict over subgroup formation, with the large groupings that allow males to compete for mating opportunities inflicting energetic and reproductive costs on females. Because association with males is central to female chimpanzees’ anti-infanticide strategy, and males may confer other benefits, we propose that reproductive success in female chimpanzees hinges on a delicate balance between the costs and benefits of associating with male conspecifics.

Animal behaviour: Incipient tradition in wild chimpanzees.

The adoption of a new form of tool use has been observed to spread along social-network pathways in a chimpanzee community. The finding offers the first direct evidence of cultural diffusion in these animals in the wild.

Social network analysis shows direct evidence for social transmission of tool use in wild chimpanzees.

Author SummaryChimpanzees are widely considered as the most “cultural” of all animals, despite the lack of direct evidence for the spread of novel behaviors through social learning in the wild. Here, we present a novel, dynamic network-based diffusion analysis to describe the acquisition patterns of novel tool-use behavior in the Sonso chimpanzee community of Budongo Forest, Uganda. We find strong evidence for social transmission of “moss-sponging” (the production of a sponge consisting of moss) along the innovators' social network, demonstrating that wild chimpanzees learn novel tool-use behaviors from each other and supporting the more general claim that some of the observed behavioral diversity in wild chimpanzees should be interpreted as “cultural.” Our model also estimated that, for each new observation, naïve individuals enhanced their chances of developing moss-sponging by a factor of 15. We conclude that group-specific behavioral variants can be socially learned in wild chimpanzees, addressing an important critique of the claim of culture in our closest relatives.

The extent of cultural variation between adjacent chimpanzee (Pan troglodytes verus) communities; A microecological approach

Chimpanzees show cultural differences among populations across Africa but also between neighboring communities. The extent of these differences among neighbors, however, remains largely unknown. Comparing three neighboring chimpanzee community in the Taï National Park, Côte d'Ivoire, we found 27 putative cultural traits, including tool use, foraging, social interaction, communication and hunting behavior, exceeding by far previously known diversity. As foraging behavior is predominantly influenced by the environment, we further compared in detail ecological circumstances underlying insectivore feeding behavior to analyze whether foraging differences on Dorylus ants and Thoracotermes termites seen between neighboring chimpanzee communities were caused by environmental factors. Differences in the prey characteristics of Dorylus ants (aggression level, running speed, and nest structure) that could influence the behavior of chimpanzees were excluded, suggesting that the observed group-specific variation is not ecologically driven. Only one community preyed on Thoracotermes termites despite a similar abundance of termite mounds in all three territories, supporting the idea that this difference is also not shaped by the environment. Therefore, our study suggests that transmission of cultural knowledge plays a role in determining insectivory prey behavior. This behavioral plasticity, independent of ecological conditions, can lead to large numbers of cultural diversification between neighboring chimpanzee communities. These findings not only deepen our understanding of the cultural abilities of chimpanzees in the wild but also open up possible future comparisons of the origin of cultural diversification among humans and chimpanzees.

Chimpanzees copy dominant and knowledgeable individuals: implications for cultural diversity

Evolutionary theory predicts that natural selection will fashion cognitive biases to guide when, and from whom, individuals acquire social information, but the precise nature of these biases, especially in ecologically valid group contexts, remains unknown. We exposed four captive groups of chimpanzees (Pan troglodytes) to a novel extractive foraging device and, by fitting statistical models, isolated four simultaneously operating transmission biases. These include biases to copy (i) higher-ranking and (ii) expert individuals, and to copy others when (iii) uncertain or (iv) of low rank. High-ranking individuals were relatively un-strategic in their use of acquired knowledge, which, combined with the bias for others to observe them, may explain reports that high innovation rates (in juveniles and subordinates) do not generate a correspondingly high frequency of traditions in chimpanzees. Given the typically low rank of immigrants in chimpanzees, a ‘copying dominants’ bias may contribute to the observed maintenance of distinct cultural repertoires in neighboring communities despite sharing similar ecology and knowledgeable migrants. Thus, a copying dominants strategy may, as often proposed for conformist transmission, and perhaps in concert with it, restrict the accumulation of traditions within chimpanzee communities whilst maintaining cultural diversity.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts.

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

Network-based vaccination improves prospects for disease control in wild chimpanzees.

Many endangered wildlife populations are vulnerable to infectious diseases for which vaccines exist; yet, pragmatic considerations often preclude large-scale vaccination efforts. These barriers could be reduced by focusing on individuals with the highest contact rates. However, the question then becomes whether targeted vaccination is sufficient to prevent large outbreaks. To evaluate the efficacy of targeted wildlife vaccinations, we simulate pathogen transmission and control on monthly association networks informed by behavioural data from a wild chimpanzee community (Kanyawara N = 37, Kibale National Park, Uganda). Despite considerable variation across monthly networks, our simulations indicate that targeting the most connected individuals can prevent large outbreaks with up to 35% fewer vaccines than random vaccination. Transmission heterogeneities might be attributed to biological differences among individuals (e.g. sex, age, dominance and family size). Thus, we also evaluate the effectiveness of a trait-based vaccination strategy, as trait data are often easier to collect than interaction data. Our simulations indicate that a trait-based strategy can prevent large outbreaks with up to 18% fewer vaccines than random vaccination, demonstrating that individual traits can serve as effective estimates of connectivity. Overall, these results suggest that fine-scale behavioural data can help optimize pathogen control efforts for endangered wildlife.

'Adoption' by maternal siblings in wild chimpanzees.

The adoption of unrelated orphaned infants is something chimpanzees and humans have in common. Providing parental care has fitness implications for both the adopter and orphan, and cases of adoption have thus been cited as evidence for a shared origin of an altruistic behaviour. We provide new data on adoptions in the free-living Sonso chimpanzee community in Uganda, together with an analysis of published data from other long-term field sites. As a default pattern, we find that orphan chimpanzees do not become adopted by adult group members but wherever possible associate with each other, usually as maternal sibling pairs. This occurs even if both partners are still immature, with older individuals effectively becoming ‘child household heads’. Adoption of orphans by unrelated individuals does occur but usually only if no maternal siblings or other relatives are present and only after significant delays. In conclusion, following the loss of their mother, orphaned chimpanzees preferentially associate along pre-existing social bonds, which are typically strongest amongst maternal siblings.

A group-specific arbitrary tradition in chimpanzees (Pan troglodytes).

Social learning in chimpanzees has been studied extensively and it is now widely accepted that chimpanzees have the capacity to learn from conspecifics through a multitude of mechanisms. Very few studies, however, have documented the existence of spontaneously emerged traditions in chimpanzee communities. While the rigour of experimental studies is helpful to investigate social learning mechanisms, documentation of naturally occurring traditions is necessary to understand the relevance of social learning in the real lives of animals. In this study, we report on chimpanzees spontaneously copying a seemingly non-adaptive behaviour ("grass-in-ear behaviour"). The behaviour entailed chimpanzees selecting a stiff, straw-like blade of grass, inserting the grass into one of their own ears, adjusting the position, and then leaving it in their ear during subsequent activities. Using a daily focal follow procedure, over the course of 1year, we observed 8 (out of 12) group members engaging in this peculiar behaviour. Importantly, in the three neighbouring groups of chimpanzees (n=82), this behaviour was only observed once, indicating that ecological factors were not determiners of the prevalence of this behaviour. These observations show that chimpanzees have a tendency to copy each other's behaviour, even when the adaptive value of the behaviour is presumably absent.

The risk of disease to great apes: simulating disease spread in orang-utan (Pongo pygmaeus wurmbii) and chimpanzee (Pan troglodytes schweinfurthii) association networks.

All great ape species are endangered, and infectious diseases are thought to pose a particular threat to their survival. As great ape species vary substantially in social organisation and gregariousness, there are likely to be differences in susceptibility to disease types and spread. Understanding the relation between social variables and disease is therefore crucial for implementing effective conservation measures. Here, we simulate the transmission of a range of diseases in a population of orang-utans in Sabangau Forest (Central Kalimantan) and a community of chimpanzees in Budongo Forest (Uganda), by systematically varying transmission likelihood and probability of subsequent recovery. Both species have fission-fusion social systems, but differ considerably in their level of gregariousness. We used long-term behavioural data to create networks of association patterns on which the spread of different diseases was simulated. We found that chimpanzees were generally far more susceptible to the spread of diseases than orang-utans. When simulating different diseases that varied widely in their probability of transmission and recovery, it was found that the chimpanzee community was widely and strongly affected, while in orang-utans even highly infectious diseases had limited spread. Furthermore, when comparing the observed association network with a mean-field network (equal contact probability between group members), we found no major difference in simulated disease spread, suggesting that patterns of social bonding in orang-utans are not an important determinant of susceptibility to disease. In chimpanzees, the predicted size of the epidemic was smaller on the actual association network than on the mean-field network, indicating that patterns of social bonding have important effects on susceptibility to disease. We conclude that social networks are a potentially powerful tool to model the risk of disease transmission in great apes, and that chimpanzees are particularly threatened by infectious disease outbreaks as a result of their social structure.

How old are chimpanzee communities? Time to the most recent common ancestor of the Y-chromosome in highly patrilocal societies

Many human societies are patrilineal, with males passing on their name or descent group affiliation to their offspring. Y-chromosomes are also passed on from father to son, leading to the simple expectation that males sharing the same surname or descent group membership should have similar Y-chromosome haplotypes. Although several studies in patrilineal human societies have examined the correspondence between Y-chromosome variation and surname or descent group membership, similar studies in non-human animals are lacking. Chimpanzees represent an excellent species for examining the relationship between descent group membership and Y-chromosome variation because they live in strongly male philopatric communities that arise by a group-fissioning process. Here we take advantage of recent analytical advances in the calculation of the time to the most recent common male ancestor and a large sample size of 273 Y-chromosome short tandem repeat haplotypes to inform our understanding of the potential ages of eight communities of chimpanzees. We find that the times to the most recent common male ancestor of chimpanzee communities are several hundred to as much as over two thousand years. These genetic estimates of the great time depths of chimpanzee communities accord well with behavioral observations suggesting that community fissions are a very rare event and are similar to genetic estimates of the time depth of patrilineal human groups.

Tradition over trend: Neighboring chimpanzee communities maintain differences in cultural behavior despite frequent immigration of adult females

The notion of animal culture has been well established mainly through research aiming at uncovering differences between populations. In chimpanzees (Pan troglodytes verus), cultural diversity has even been found in neighboring communities, where differences were observed despite frequent immigration of individuals. Female chimpanzees transfer at the onset of sexual maturity at an age, when the behavioral repertoire is fully formed. With immigrating females, behavioral variety enters the group. Little is known about the diversity and the longevity of cultural traits within a community. This study is building on previous findings of differences in hammer selection when nut cracking between neighboring communities despite similar ecological conditions. We now further investigated the diversity and maintenance of cultural traits within one chimpanzee community and were able to show high levels of uniformity in group-specific behavior. Fidelity to the behavior pattern did not vary between dispersing females and philopatric males. Furthermore, group-specific tool selection remained similar over a period of 25 years. Additionally, we present a study case on how one newly immigrant female progressively behaved more similar to her new group, suggesting that the high level of similarity in behavior is actively adopted by group members possibly even when originally expressing the behavior in another form. Taken together, our data support a cultural transmission process in adult chimpanzees, which leads to persisting cultural behavior of one community over time.

Genetic analyses suggest no immigration of adult females and their offspring into the Sonso community of chimpanzees in the Budongo Forest Reserve, Uganda

Chimpanzees are frequently used to illustrate the relationship between sex differences in dispersal and sex differences in cooperation in primates and other group-living mammals. Male chimpanzees are highly philopatric, typically remaining in their natal communities for their entire lives to cooperate with related males in competition against less related males from other groups, whereas females typically disperse once at adolescence and cooperate with each other less frequently. However, there have been a few reports of dependent male offspring joining groups when their mothers transferred between communities as adults. Although such events are difficult to document, determining how often they actually occur is important for elucidating the links between philopatry, kinship, and cooperation in both chimpanzees and group-living animals more generally. Here we use genetic analyses to investigate a previous report of a large-scale transfer of many females and their offspring into the Sonso community of chimpanzees in the Budongo Forest Reserve, Uganda. Using autosomal microsatellite genotypes, we assigned a Sonso father to ten of the fourteen putative immigrants, and found that the four putative immigrants for whom we could not assign a Sonso father (perhaps due to incomplete sampling of all Sonso candidate fathers) nevertheless had Y-chromosome microsatellite haplotypes that were common in Sonso males but absent in males from four other chimpanzee communities at Budongo. These results suggest that these putative immigrant females and their offspring were probably actually long-term residents of Sonso whose identifications were delayed by their peripheral or unhabituated status. These results are consistent with other genetic and behavioral evidence showing that male between-community gene flow is exceedingly rare in east African chimpanzees.

Deictic gesturing in wild chimpanzees (Pan troglodytes)? Some possible cases.

Referential pointing is important in the development of language comprehension in the child and is often considered a uniquely human capacity. Nonhuman great apes do point in captivity, usually for a human audience, but this has been interpreted as an interaction pattern learned from human caretakers, not indicative of natural deictic ability. In contrast, spontaneous pointing for other apes is almost unknown among wild ape populations, supporting doubts as to whether apes naturally have any capacity to point referentially. Here the authors describe and illustrate 4 cases of gestures by juvenile chimpanzees in the Sonso chimpanzee community in Budongo, Uganda, that, at some level, may appear to be deictic and referential. The authors discuss the possible reasons why chimpanzees, if they possess a capacity for referential pointing, do not use it more frequently.

Predicting the vulnerability of great apes to disease: the role of superspreaders and their potential vaccination.

Disease is a major concern for the conservation of great apes, and one that is likely to become increasingly relevant as deforestation and the rise of ecotourism bring humans and apes into ever closer proximity. Consequently, it is imperative that preventative measures are explored to ensure that future epidemics do not wipe out the remaining populations of these animals. In this paper, social network analysis was used to investigate vulnerability to disease in a population of wild orang-utans and a community of wild chimpanzees. Potential ‘superspreaders’ of disease - individuals with disproportionately central positions in the community or population - were identified, and the efficacy of vaccinating these individuals assessed using simulations. Three resident female orang-utans were identified as potential superspreaders, and females and unflanged males were predicted to be more influential in disease spread than flanged males. By contrast, no superspreaders were identified in the chimpanzee network, although males were significantly more central than females. In both species, simulating the vaccination of the most central individuals in the network caused a greater reduction in potential disease pathways than removing random individuals, but this effect was considerably more pronounced for orang-utans. This suggests that targeted vaccinations would have a greater impact on reducing disease spread among orang-utans than chimpanzees. Overall, these results have important implications for orang-utan and chimpanzee conservation and highlight the role that certain individuals may play in the spread of disease and its prevention by vaccination.

Chimpanzee fauna isotopes provide new interpretations of fossil ape and hominin ecologies

Carbon and oxygen stable isotopes within modern and fossil tooth enamel record the aspects of an animal's diet and habitat use. This investigation reports the first isotopic analyses of enamel from a large chimpanzee community and associated fauna, thus providing a means of comparing fossil ape and early hominin palaeoecologies with those of a modern ape. Within Kibale National Park forest, oxygen isotopes differentiate primate niches, allowing for the first isotopic reconstructions of degree of frugivory versus folivory as well as use of arboreal versus terrestrial resources. In a comparison of modern and fossil community isotopic profiles, results indicate that Sivapithecus, a Miocene ape from Pakistan, fed in the forest canopy, as do chimpanzees, but inhabited a forest with less continuous canopy or fed more on leaves. Ardipithecus, an early hominin from Ethiopia, fed both arboreally and terrestrially in a more open habitat than inhabited by chimpanzees.

Co-residence between males and their mothers and grandmothers is more frequent in bonobos than chimpanzees.

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.

Genetic diversity at the edge: comparative assessment of Y-chromosome and autosomal diversity in eastern chimpanzees (Pan troglodytes schweinfurthii) of Ugalla, Tanzania

One of the three categories of biodiversity for conservation priority recommended by the International Union for the Conservation of Nature is genetic diversity. In this study, we estimate the genetic diversity of eastern chimpanzees in the Ugalla region of western Tanzania, which represents the easternmost distribution of the subspecies Pan troglodytes schweinfurthii. We collected 237 fecal samples from a 624 km2 area of the Ugalla region, analyzed the DNA at 12 autosomal loci and identified 113 individuals (69 males and 44 females). We also analyzed 13 Y-chromosome loci in the Ugalla males. While autosomal genetic diversity is within the range of other eastern populations, at 0.27 the gene diversity of the Y-chromosome haplotypes present among 61 Ugalla males is extremely low as compared to other eastern chimpanzee populations. In addition, the most prevalent haplotype, found in 52 of the males, is distributed across the entire surveyed area of 624 km2. This low level of paternally-transmitted genetic diversity among the Ugalla males may be the result of a small or highly related, recent founder population (i.e., genetic drift), exacerbated by the male philopatric structure of chimpanzee communities and by male reproductive skew.

Female competition in chimpanzees.

Female chimpanzees exhibit exceptionally slow rates of reproduction and raise their offspring without direct paternal care. Therefore, their reproductive success depends critically on long-term access to high-quality food resources over a long lifespan. Chimpanzee communities contain multiple adult males, multiple adult females and their offspring. Because males are philopatric and jointly defend the community range while most females transfer to new communities before breeding, adult females are typically surrounded by unrelated competitors. Communities are fission-fusion societies in which individuals spend time alone or in fluid subgroups, whose size depends mostly on the abundance and distribution of food. To varying extents in different populations, females avoid direct competition by foraging alone or in small groups in distinct, but overlapping core areas within the community range to which they show high fidelity. Although rates of aggression are low, females compete for space and access to food. High rank correlates with high reproductive success, and high-ranking females win direct contests for food and gain preferential access to resource-rich sites. Females are aggressive to immigrant females and even kill the newborn infants of community members. The intensity of such aggression correlates with population density. These patterns are compared to those in other species, including humans.

Locomotor and postural development of wild chimpanzees

Chimpanzees are our closest living relatives and their positional repertoire likely includes elements shared with our common ancestor. Currently, limitations exist in our ability to correlate locomotor anatomy with behavioral function in the wild. Here we provide a detailed description of developmental changes in chimpanzee locomotion and posture. Fieldwork was conducted on wild chimpanzees at Ngogo, Kibale National Park, Uganda. The large size of the Ngogo chimpanzee community permitted cross-sectional analysis of locomotor and postural changes across many individuals. Chimpanzee positional behavior proceeds developmentally through a number of distinct stages, each characterized by its own loading regime. Infants principally used their upper limbs while moving; the loading environment changed to more hindlimb dominated locomotion as infants aged. Infants displayed more diversity in their forms of positional behavior than members of any other age-sex class, engaging in behaviors not habitually exhibited by adults. While the most common locomotor mode for infants was torso-orthograde suspensory locomotion, a large shift toward quadrupedal locomotion during infancy occurred at three years of age, when rates of this behavior increased. Overall, the most dramatic transition in positional behavior occurred during juvenility (at approximately five years), with the advent of complete independent locomotion. Juveniles decreased the amount of time they spent clinging and in torso-orthograde suspensory locomotion and increased their time spent sitting and walking and running quadrupedally compared with younger individuals. Juvenility marked the age at which quadrupedal walking became the most frequent locomotor behavior, but quadrupedal walking did not encompass the majority of locomotor time until individuals reached adolescence. Relative to all younger individuals, adolescent chimpanzees (10–13 years) experienced a further increase in the amount of time they walked quadrupedally. Locomotor behavior did not reach adult form until adolescence, closer to the time of epiphyseal fusion than previously thought. These findings provide new data to make predictions about how behavioral transitions influence skeletal change.