Flexible grouping patterns in a western and eastern chimpanzee community.

Primate social organizations, or grouping patterns, vary significantly across species. Behavioral strategies that allow for flexibility in grouping patterns offer a means to reduce the costs of group living. Chimpanzees (Pan troglodytes) have a fission-fusion social system in which temporary subgroups ("parties") change in composition because of local socio-ecological conditions. Notably, western chimpanzees (P. t. verus) are described as showing a higher degree of bisexual bonding and association than eastern chimpanzees, and eastern female chimpanzees (P. t. schweinfurthii) are thought to be more solitary than western female chimpanzees. However, reported comparisons in sociality currently depend on a small number of study groups, particularly in western chimpanzees, and variation in methods. The inclusion of additional communities and direct comparison using the same methods are essential to assess whether reported subspecies differences in sociality hold in this behaviorally heterogeneous species. We explored whether sociality differs between two communities of chimpanzees using the same motion-triggered camera technology and definitions of social measures. We compare party size and composition (party type, sex ratio) between the western Gahtoy community in the Nimba Mountains (Guinea) and the eastern Waibira community in the Budongo Forest (Uganda). Once potential competition for resources such as food and mating opportunities were controlled for, subspecies did not substantially influence the number of individuals in a party. We found a higher sex-ratio, indicating more males in a party, in Waibira; this pattern was driven by a greater likelihood in Gahtoy to be in all-female parties. This finding is the opposite of what was expected for eastern chimpanzees, where female-only parties are predicted to be more common. Our results highlight the flexibility in chimpanzee sociality, and caution against subspecies level generalizations.

To drum or not to drum: Selectivity in tree buttress drumming by chimpanzees (Pan troglodytes verus) in the Nimba Mountains, Guinea.

Chimpanzees live in fission-fusion social organizations, which means that party size, composition, and spatial distribution are constantly in flux. Moreover, chimpanzees use a remarkably extensive repertoire of vocal and nonvocal forms of communication, thought to help convey information in such a socially and spatially dynamic setting. One proposed form of nonvocal communication in chimpanzees is buttress drumming, in which an individual hits a tree buttress with its hands and/or feet, thereby producing a low-frequency acoustic signal. It is often presumed that this behavior functions to communicate over long distances and is, therefore, goal-oriented. If so, we would expect chimpanzees to exhibit selectivity in the choice of trees and buttresses used in buttress drumming. Selectivity is a key attribute of many other goal-directed chimpanzee behaviors, such as nut-cracking and ant dipping. Here, we investigate whether chimpanzees at the Seringbara study site in the Nimba Mountains, Guinea, West Africa, show selectivity in their buttress drumming behavior. Our results indicate that Seringbara chimpanzees are more likely to use larger trees and select buttresses that are thinner and have a greater surface area. These findings imply that tree buttress drumming is not a random act, but rather goal-oriented and requires knowledge of suitable trees and buttresses. Our results also point to long-distance communication as a probable function of buttress drumming based on selectivity for buttress characteristics likely to impact sound propagation. This study provides a foundation for further assessing the cognitive underpinnings and functions of buttress drumming in wild chimpanzees.

CD4 receptor diversity in chimpanzees protects against SIV infection.

Human and simian immunodeficiency viruses (HIV/SIVs) use CD4 as the primary receptor to enter target cells. Here, we show that the chimpanzee CD4 is highly polymorphic, with nine coding variants present in wild populations, and that this diversity interferes with SIV envelope (Env)-CD4 interactions. Testing the replication fitness of SIVcpz strains in CD4+ T cells from captive chimpanzees, we found that certain viruses were unable to infect cells from certain hosts. These differences were recapitulated in CD4 transfection assays, which revealed a strong association between CD4 genotypes and SIVcpz infection phenotypes. The most striking differences were observed for three substitutions (Q25R, Q40R, and P68T), with P68T generating a second N-linked glycosylation site (N66) in addition to an invariant N32 encoded by all chimpanzee CD4 alleles. In silico modeling and site-directed mutagenesis identified charged residues at the CD4-Env interface and clashes between CD4- and Env-encoded glycans as mechanisms of inhibition. CD4 polymorphisms also reduced Env-mediated cell entry of monkey SIVs, which was dependent on at least one D1 domain glycan. CD4 allele frequencies varied among wild chimpanzees, with high diversity in all but the western subspecies, which appeared to have undergone a selective sweep. One allele was associated with lower SIVcpz prevalence rates in the wild. These results indicate that substitutions in the D1 domain of the chimpanzee CD4 can prevent SIV cell entry. Although some SIVcpz strains have adapted to utilize these variants, CD4 diversity is maintained, protecting chimpanzees against infection with SIVcpz and other SIVs to which they are exposed.

Open-access platform to synthesize knowledge of ape conservation across sites.

Despite the large body of literature on ape conservation, much of the data needed for evidence-based conservation decision-making is still not readily accessible and standardized, rendering cross-site comparison difficult. To support knowledge synthesis and to complement the IUCN SSC Ape Populations, Environments and Surveys database, we created the A.P.E.S. Wiki (https://apeswiki.eva.mpg.de), an open-access platform providing site-level information on ape conservation status and context. The aim of this Wiki is to provide information and data about geographical ape locations, to curate information on individuals and organizations active in ape research and conservation, and to act as a tool to support collaboration between conservation practitioners, scientists, and other stakeholders. To illustrate the process and benefits of knowledge synthesis, we used the momentum of the update of the conservation action plan for western chimpanzees (Pan troglodytes verus) and began with this critically endangered taxon. First, we gathered information on 59 sites in West Africa from scientific publications, reports, and online sources. Information was compiled in a standardized format and can thus be summarized using a web scraping approach. We then asked experts working at those sites to review and complement the information (20 sites have been reviewed to date). We demonstrate the utility of the information available through the Wiki, for example, for studying species distribution. Importantly, as an open-access platform and based on the well-known wiki layout, the A.P.E.S. Wiki can contribute to direct and interactive information sharing and promote the efforts invested by the ape research and conservation community. The Section on Great Apes and the Section on Small Apes of the IUCN SSC Primate Specialist Group will guide and support the expansion of the platform to all small and great ape taxa. Similar collaborative efforts can contribute to extending knowledge synthesis to all nonhuman primate species.

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.

Crab-fishing by chimpanzees in the Nimba Mountains, Guinea.

The significance of aquatic food resources for hominins is poorly understood, despite evidence of consumption as early as 1.95 million years ago (Ma). Here we present the first evidence of a non-human ape habitually catching and consuming aquatic crabs. Chimpanzees (Pan troglodytes verus) in the rainforest of the Nimba Mountains (Guinea) consumed freshwater crabs year-round, irrespective of rainfall or ripe fruit availability. Parties of females and offspring fished for crabs more than predicted and for longer durations than adult males. Across months, crab-fishing was negatively correlated with ant-dipping, suggesting a similar nutritional role. These findings contribute to our understanding of aquatic faunivory among hominins. First, aquatic faunivory can occur in closed forests in addition to open wetlands. Second, aquatic fauna could have been a staple part of some hominin diets, rather than merely a fallback food. Third, the habitual consumption of aquatic fauna could have been especially important for females and their immature offspring. In addition to providing small amounts of essential fatty acids, crabs might also be eaten for their micronutrients such as sodium and calcium, especially by females and young individuals who may have limited access to meat.

Chimpanzees prey on army ants at Seringbara, Nimba Mountains, Guinea: predation patterns and tool use characteristics.

Chimpanzees are renowned for their use of foraging tools in harvesting social insects and some populations use tools to prey on aggressive army ants (Dorylus spp.). Tool use in army ant predation varies across chimpanzee study sites with differences in tool length, harvesting technique, and army ant species targeted. However, surprisingly little is known about the detailed ecology of army ant predation. We studied army ant predation by chimpanzees (Pan troglodytes verus) at the Seringbara study site in the Nimba Mountains, Guinea (West Africa), over 10 years (2003-2013). We investigated chimpanzee selectivity with regards to army ant prey species. We assessed the temporal variation in army ant-feeding and examined whether army ant predation was related to rainfall or ripe fruit availability. Moreover, we examined whether chimpanzees showed selectivity regarding plant species used for tool manufacture, as well as the relationship between tool species preference and tool collection distance. Lastly, we measured tool properties and investigated the use of tool sets and composite tools in army ant predation. Seringbara chimpanzees preyed on one army ant species (D. nigricans) more often than expected based on encounter rates, which may be explained by the overlap in altitudinal distribution between chimpanzees and D. nigricans. Army ant predation was not related to rainfall or fruit availability. Chimpanzees were selective in their choice of tool materials and collected their preferred tool species (Alchornea hirtella) from greater distances than they did other species. Lastly, Seringbara chimpanzees used both tool sets and composite tools (tree perch) in army ant predation. Tool types (dig vs. dip) differed in width and strength, but not length. Tool composites were found at 40% of ant-feeding sites. Our study sheds new light on the ecology of army ant predation and provides novel insights into chimpanzee selection of army ant prey and tool species.

The ecology of primate material culture.

Tool use in extant primates may inform our understanding of the conditions that favoured the expansion of hominin technology and material culture. The 'method of exclusion' has, arguably, confirmed the presence of culture in wild animal populations by excluding ecological and genetic explanations for geographical variation in behaviour. However, this method neglects ecological influences on culture, which, ironically, may be critical for understanding technology and thus material culture. We review all the current evidence for the role of ecology in shaping material culture in three habitual tool-using non-human primates: chimpanzees, orangutans and capuchin monkeys. We show that environmental opportunity, rather than necessity, is the main driver. We argue that a better understanding of primate technology requires explicit investigation of the role of ecological conditions. We propose a model in which three sets of factors, namely environment, sociality and cognition, influence invention, transmission and retention of material culture.

Terrestrial nest-building by wild chimpanzees (Pan troglodytes): implications for the tree-to-ground sleep transition in early hominins.

Nest-building is a great ape universal and arboreal nesting in chimpanzees and bonobos suggests that the common ancestor of Pan and Homo also nested in trees. It has been proposed that arboreal nest-building remained the prevailing pattern until Homo erectus, a fully terrestrial biped, emerged. We investigated the unusual occurrence of ground-nesting in chimpanzees (Pan troglodytes), which may inform on factors influencing the tree-to-ground sleep transition in the hominin lineage. We used a novel genetic approach to examine ground-nesting in unhabituated chimpanzees at Seringbara in the Nimba Mountains, Guinea. Previous research showed that ground-nesting at Seringbara was not ecologically determined. Here, we tested a possible mate-guarding function of ground-nesting by analyzing DNA from shed hairs collected from ground nests and tree nests found in close proximity. We examined whether or not ground-nesting was a group-level behavioral pattern and whether or not it occurred in more than one community. We used multiple genetic markers to identify sex and to examine variation in mitochondrial DNA control region (HV1, HV2) sequences. Ground-nesting was a male-biased behavior and males constructed more elaborate ("night") nests than simple ("day") nests on the ground. The mate-guarding hypothesis was not supported, as ground and associated tree nests were built either by maternally-related males or possibly by the same individuals. Ground-nesting was widespread and likely habitual in two communities. We suggest that terrestrial nest-building may have already occurred in arboreally-adapted early hominins before the emergence of H. erectus.

Animal behavior: Monkeys use tools for diet quality, not quantity.

An enduring question in the study of human evolution is why tool use evolved. A new study has found that stone tools improve diet quality in wild capuchin monkeys. Tools may have similarly increased the nutritional security in ancestral hominins.

Field experiments find no evidence that chimpanzee nut cracking can be independently innovated.

Cumulative culture has been claimed a hallmark of human evolution. Yet, the uniqueness of human culture is heavily debated. The zone of latent solutions hypothesis states that only humans have cultural forms that require form-copying social learning and are culture-dependent. Non-human ape cultural behaviours are considered 'latent solutions', which can be independently (re-)innovated. Others claim that chimpanzees, like humans, have cumulative culture. Here, we use field experiments at Seringbara (Nimba Mountains, Guinea) to test whether chimpanzee nut cracking can be individually (re-)innovated. We provided: (1) palm nuts and stones, (2) palm fruit bunch, (3) cracked palm nuts and (4) Coula nuts and stones. Chimpanzee parties visited (n = 35) and explored (n = 11) the experiments but no nut cracking occurred. In these experiments, chimpanzees did not individually (re-)innovate nut cracking under ecologically valid conditions. Our null results are consistent with the hypothesis that chimpanzee nut cracking is a product of social learning.

The evolutionary drivers of primate scleral coloration.

The drivers of divergent scleral morphologies in primates are currently unclear, though white sclerae are often assumed to underlie human hyper-cooperative behaviours. Humans are unusual in possessing depigmented sclerae whereas many other extant primates, including the closely-related chimpanzee, possess dark scleral pigment. Here, we use phylogenetic generalized least squares (PGLS) analyses with previously generated species-level scores of proactive prosociality, social tolerance (both n = 15 primate species), and conspecific lethal aggression (n = 108 primate species) to provide the first quantitative, comparative test of three existing hypotheses. The 'self-domestication' and 'cooperative eye' explanations predict white sclerae to be associated with cooperative, rather than competitive, environments. The 'gaze camouflage' hypothesis predicts that dark scleral pigment functions as gaze direction camouflage in competitive social environments. Notably, the experimental evidence that non-human primates draw social information from conspecific eye movements is unclear, with the latter two hypotheses having recently been challenged. Here, we show that white sclerae in primates are associated with increased cooperative behaviours whereas dark sclerae are associated with reduced cooperative behaviours and increased conspecific lethal violence. These results are consistent with all three hypotheses of scleral evolution, suggesting that primate scleral morphologies evolve in relation to variation in social environment.

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs.

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.

How to measure chimpanzee party size? A methodological comparison.

Chimpanzees (Pan troglodytes) live in fission-fusion societies where community members form temporary parties that frequently change in size and composition. Chimpanzee party size and composition have been widely studied to identify proximate causes of grouping patterns, and party size estimates are used to assess population sizes and densities. Numerous socio-ecological factors influence chimpanzee party size, but findings differ across studies. Various methods to measure party size exist, including direct observations, motion-triggered camera (MTC) observations, and nest counts. However, comparative analyses of these methods are lacking. Here, we assess relative differences in four commonly used party size methods and we examine socio-ecological factors influencing party size of unhabituated chimpanzees (P. t. verus) at Seringbara, Nimba, Guinea. We also assess which method(s) best reflect the influence of socio-ecological factors on party size. Using data collected over 69 months, we show that night nest counts resulted in relatively larger party size estimates than the other methods, and day nest counts resulted in relatively smaller party size estimates. Direct and MTC observations did not differ in relative estimates of party size and composition. Both fruit abundance and presence of estrous females positively influenced party size, but this effect was only evident when measuring party size with MTCs. Methods thus differ in relative party size estimates and their ability to assess the impact of socio-ecological factors. We conclude that MTC observations best represent party size and the effect of socio-ecological factors at Nimba. MTCs show promising potential for studying grouping patterns in unhabituated chimpanzees.

Modeling habitat suitability for chimpanzees (Pan troglodytes verus) in the Greater Nimba Landscape, Guinea, West Africa.

Tropical forests and the biodiversity within them are rapidly declining in the face of increasing human populations. Resource management and conservation of endangered species requires an understanding of how species perceive and respond to their environments. Species distribution modeling (SDM) is an appropriate tool for identifying conservation areas of concern and importance. In this study, SDM was used to identify areas of suitable chimpanzee (Pan troglodytes verus) habitat within the Greater Nimba Landscape, Guinea, West Africa. This location was ideal for investigating the effects of landscape structure on habitat suitability due to the topographic variation of the landscape and the Critically Endangered status of the Western chimpanzee. Additionally, this is the only mountainous, long-term chimpanzee study site and little is known about the effects of topography on chimpanzee behavior. Suitable habitat was predicted based on the location of direct and indirect signs of chimpanzee presence and the spatial distribution of 12 biophysical variables within the study area. Model performance was assessed by examining the area under the curve. The overall predictive performance of the model was 0.721. The variables most influencing habitat suitability were the normalized difference vegetation index (37.8%), elevation (27.3%), hierarchical slope position (11.5%), surface brightness (6.6%), and distance to rivers (5.4%). The final model highlighted the isolation and fragmentation of chimpanzee habitat within the Greater Nimba Landscape. Understanding the factors influencing chimpanzee habitat suitability, specifically the biophysical variables considered in this study, will greatly contribute to conservation efforts by providing quantitative habitat information and improving survey efficiency.

Response to: Chimpanzee culture extends beyond matrilineal family units.

We thank van Leeuwen et al.[1] for their response to our finding that matrilineal relationships strongly influence the style of high-arm grooming in wild chimpanzees of the Kanyawara community. We agree with them that grooming styles could be transmitted by different mechanisms in different contexts, and we appreciate their effort to assess whether the transmission of grooming styles within two captive groups in Chimfunshi accords with our result.

Distribution of a Chimpanzee Social Custom Is Explained by Matrilineal Relationship Rather Than Conformity.

High-arm grooming is a form of chimpanzee grooming in which two individuals mutually groom while each raising one arm. Palm-to-palm clasping (PPC) is a distinct style of high-arm grooming in which the grooming partners clasp each other's raised palms. In wild communities, samples of at least 100 observed dyads grooming with raised hands showed PPC frequencies varying from <5% (M group, Mahale) to >30% dyads grooming (Kanyawara, Kibale), and in a large free-ranging sanctuary group, the frequency reached >80% dyads (group 1, Chimfunshi) [1, 2]. Because between-community differences in frequency of PPC apparently result from social learning, are stable across generations, and last for at least 9 years, they are thought to be cultural, but the mechanism of transmission is unknown [2]. Here, we examine factors responsible for individual variation in PPC frequency within a single wild community. We found that in the Kanyawara community (Kibale, Uganda), adults of both sexes varied widely in their PPC frequency (from <10% to >50%) and did not converge on a central group tendency. However, frequencies of PPC were highly consistent within matrilines, indicating that individuals maintained lifelong fidelity to the grooming style of their mothers. Matrilineal inheritance of socially learned behaviors has previously been reported for tool use in chimpanzees [3] and in the vocal and feeding behavior of cetaceans [4, 5]. Our evidence indicates that matrilineal inheritance can be sufficiently strong in nonhuman primates to account for long-term differences in community traditions.