Camera traps unveil demography, social structure, and home range of six unhabituated Western chimpanzee groups in the Moyen Bafing National Park, Guinea.

Precise estimates of population dynamics and social grouping patterns are required for effective conservation of wild animal populations. It is difficult to obtain such information on non-human great apes as they have slow reproductive rates. To gain a better understanding of demography in these populations, previous research has typically involved habituation\, a process that requires years. Here, we collected data continuously over year-long periods to monitor an unhabituated population of critically endangered Western chimpanzees (Pan troglodytes verus) in the Moyen Bafing National Park, Guinea. We used two arrays of 100 camera traps that were placed opportunistically in two distinct 100 km2 sites, named Bakoun and Koukoutamba. We identified 227 individuals in Bakoun and 207 in Koukoutamba through their unique facial features. Our camera trap data make clear that these individuals belong to six and seven closed groups, respectively. Six of those groups were near-completely sampled with an average minimum size of 46.8 individuals (range: 37-58), and a mean adult sex ratio of 1.32 (range: 0.93-2.10). We described the demographic composition of these groups and use Bayesian social network analysis to understand population structure. The network analyses suggested that the social bonds within the two populations were structured by sex homophily, with male chimpanzees being more or equally likely to be observed together than other adult associations. Through estimation of minimum convex polygons, we described the minimum home range for those groups. Compared to other chimpanzee groups living in a similar environment (mosaic savanna-forest), the Moyen Bafing region seems to host a high-density of chimpanzees with small home ranges for their group size. Our research highlights the potential of camera traps for studying the demographic composition of chimpanzee populations with high resolution and obtaining crucial information on several groups in a time-efficient and cost-effective way.

Animal reactivity to camera traps and its effects on abundance estimate using distance sampling in the Taï National Park, Côte d'Ivoire.

The use of camera traps (CTs) has become an increasingly popular method of studying wildlife, as CTs are able to detect rare, nocturnal, and elusive species in remote and difficult-to-access areas. It thus makes them suited to estimate animal density and abundance, identify activity patterns and new behaviours of animals. However, animals can react when they see the CTs and this can lead to bias in the animal population estimates. While CTs may provide many advantages, an improved understanding of their impacts on individual's behaviour is necessary to avoid erroneous density estimates. Yet, the impact of CTs on detected individuals, such as human odour near the device and the environment, or the infrared illumination, has received relatively little attention. To date, there is no clear procedure to remove this potential bias. Here, we use camera trap distance sampling (CTDS) to (1) quantify the bias resulting from the different animal responses to the CTs when determining animal density and abundance, and (2) test if olfactory, visual and auditory signals have an influence on the animals' reaction to CTs. Between March 2019 and March 2020, we deployed CTs at 267 locations distributed systematically over the entire Taï National Park. We obtained 58,947 videos from which we analysed four medium- to-large-bodied species (Maxwell's duiker (Philantomba maxwellii), Jentink's duiker (Cephalophus jentinki), pygmy hippopotamus (Choeropsis liberiensis) and Western chimpanzee (Pan troglodytes verus)) displaying different behaviours towards the CTs. We then established species-specific ethograms describing the behavioural responses to the CTs. Using these species-specific responses, we observed that the Maxwell's duiker reacted weakly to CTs (about 0.11% of the distance data), contrary to Jentink's duiker, pygmy hippopotamus and Western chimpanzee which reacted with relatively high frequencies, representing 32.82%, 52.96% and 16.14% of the distance data, respectively. Not taking into account the species-specific responses to the CTs can lead to an artificial doubling or tripling of the populations' sizes. All species reacted more to the CTs at close distances. Besides, the Jentink's duiker and the pygmy hippopotamus reacted significantly more to the CTs at night than during the day. Finally, as for olfactory signals, the probability of reaction to the CTs during the first days after CTs installation was weak in Maxwell's duiker, but concerned 18% of the video captures in Western chimpanzees which decreasing with time, but they remained high in pygmy hippopotamus and Jentink's duiker (65% and 70% of the video captures respectively). Careful consideration should be given to animal's response to CTs during the analysis and in the field, by reducing human's impact around the CTs installation.

Range-wide indicators of African great ape density distribution.

Species distributions are influenced by processes occurring at multiple spatial scales. It is therefore insufficient to model species distribution at a single geographic scale, as this does not provide the necessary understanding of determining factors. Instead, multiple approaches are needed, each differing in spatial extent, grain, and research objective. Here, we present the first attempt to model continent-wide great ape density distribution. We used site-level estimates of African great ape abundance to (1) identify socioeconomic and environmental factors that drive densities at the continental scale, and (2) predict range-wide great ape density. We collated great ape abundance estimates from 156 sites and defined 134 pseudo-absence sites to represent additional absence locations. The latter were based on locations of unsuitable environmental conditions for great apes, and on existing literature. We compiled seven socioeconomic and environmental covariate layers and fitted a generalized linear model to investigate their influence on great ape abundance. We used an Akaike-weighted average of full and subset models to predict the range-wide density distribution of African great apes for the year 2015. Great ape densities were lowest where there were high Human Footprint and Gross Domestic Product values; the highest predicted densities were in Central Africa, and the lowest in West Africa. Only 10.7% of the total predicted population was found in the International Union for Conservation of Nature Category I and II protected areas. For 16 out of 20 countries, our estimated abundances were largely in line with those from previous studies. For four countries, Central African Republic, Democratic Republic of the Congo, Liberia, and South Sudan, the estimated populations were excessively high. We propose further improvements to the model to overcome survey and predictor data limitations, which would enable a temporally dynamic approach for monitoring great apes across their range based on key indicators.

Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees.

Here we show that sexual signaling affects patterns of female spatial association differently in chimpanzees and bonobos, indicating its relevance in shaping the respective social systems. Generally, spatial association between females often mirrors patterns and strength of social relationships and cooperation within groups. While testing for proposed differences in female-female associations underlying female coalition formation in the species of the genus Pan, we find only limited evidence for a higher female-female gregariousness in bonobos. While bonobo females exhibited a slightly higher average number of females in their parties, there is neither a species difference in the time females spent alone, nor in the number of female party members in the absence of sexually attractive females. We find that the more frequent presence of maximally tumescent females in bonobos is associated with a significantly stronger increase in the number of female party members, independent of variation in a behavioural proxy for food abundance. This indicates the need to look beyond ecology when explaining species differences in female sociality as it refutes the idea that the higher gregariousness among bonobo females is driven by ecological factors alone and highlights that the temporal distribution of female sexual receptivity is an important factor to consider when studying mammalian sociality.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Identifying animal complex cognition requires natural complexity.

The search for human cognitive uniqueness often relied on low ecological tests with subjects experiencing unnatural ontogeny. Recently, neuroscience demonstrated the significance of a rich environment on the development of brain structures and cognitive abilities. This stresses the importance to consider the prior knowledge that subjects bring in any experiment. Second, recent developments in multivariate statistics control precisely for a number of factors and their interactions. Making controls in natural observations equivalent and sometimes superior to captive experimental studies without the drawbacks of the latter methods. Thus, we can now investigate complex cognition by accounting for many different factors, as required when solving tasks in nature. Combining both progresses allows us to move toward an "experience-specific cognition", recognizing that cognition varies extensively in nature as individuals adapt to the precise challenges they experience in life. Such cognitive specialization makes cross-species comparisons more complex, while potentially identifying human cognitive uniqueness.

Chimpanzee identification and social network construction through an online citizen science platform.

Citizen science has grown rapidly in popularity in recent years due to its potential to educate and engage the public while providing a means to address a myriad of scientific questions. However, the rise in popularity of citizen science has also been accompanied by concerns about the quality of data emerging from citizen science research projects. We assessed data quality in the online citizen scientist platform Chimp&See, which hosts camera trap videos of chimpanzees (Pan troglodytes) and other species across Equatorial Africa. In particular, we compared detection and identification of individual chimpanzees by citizen scientists with that of experts with years of experience studying those chimpanzees. We found that citizen scientists typically detected the same number of individual chimpanzees as experts, but assigned far fewer identifications (IDs) to those individuals. Those IDs assigned, however, were nearly always in agreement with the IDs provided by experts. We applied the data sets of citizen scientists and experts by constructing social networks from each. We found that both social networks were relatively robust and shared a similar structure, as well as having positively correlated individual network positions. Our findings demonstrate that, although citizen scientists produced a smaller data set based on fewer confirmed IDs, the data strongly reflect expert classifications and can be used for meaningful assessments of group structure and dynamics. This approach expands opportunities for social research and conservation monitoring in great apes and many other individually identifiable species.

Limited evidence of C4 plant consumption in mound building Macrotermes termites from savanna woodland chimpanzee sites.

Stable isotope analysis is an increasingly used molecular tool to reconstruct the diet and ecology of elusive primates such as unhabituated chimpanzees. The consumption of C4 plant feeding termites by chimpanzees may partly explain the relatively high carbon isotope values reported for some chimpanzee communities. However, the modest availability of termite isotope data as well as the diversity and cryptic ecology of termites potentially consumed by chimpanzees obscures our ability to assess the plausibility of these termites as a C4 resource. Here we report the carbon and nitrogen isotope values from 79 Macrotermes termite samples from six savanna woodland chimpanzee research sites across equatorial Africa. Using mixing models, we estimated the proportion of Macrotermes C4 plant consumption across savanna woodland sites. Additionally, we tested for isotopic differences between termite colonies in different vegetation types and between the social castes within the same colony in a subset of 47 samples from 12 mounds. We found that Macrotermes carbon isotope values were indistinguishable from those of C3 plants. Only 5 to 15% of Macrotermes diets were comprised of C4 plants across sites, suggesting that they cannot be considered a C4 food resource substantially influencing the isotope signatures of consumers. In the Macrotermes subsample, vegetation type and caste were significantly correlated with termite carbon values, but not with nitrogen isotope values. Large Macrotermes soldiers, preferentially consumed by chimpanzees, had comparably low carbon isotope values relative to other termite castes. We conclude that Macrotermes consumption is unlikely to result in high carbon isotope values in either extant chimpanzees or fossil hominins.

Lessons learned while protecting wild chimpanzees in West Africa.

Though human activities are postulated to be the main drivers of the worldwide biodiversity crisis, humans are also suggested by some to be an important part of the solution to the crisis. How can such a paradox be best solved? This paradox requires an adaptive, context-specific, dynamic solution, at a fine-grained scale that varies by location. The Wild Chimpanzee Foundation (WCF) works on the ground in three West African countries: In Côte d'Ivoire, where bushmeat consumption is a recurrent and generalized threat to wildlife, WCF used live theater performances in the villages to address this issue. Post-activity evaluations revealed that the more often individuals have been part of such awareness activities, the less they will consume bushmeat. In nearby Liberia, where illegal miners have invaded many protected areas and intact forests, the WCF supports Community Watch Teams (CWT) to patrol the Sapo National Park with Forestry Development Authority staff. Within 11 months of its creation, the CWT patrols around and in the Sapo National Park resulted in thousands of illegal miners progressively leaving the national park. In Guinea, where coexistence between humans and primates has prevailed based on religious traditions, the WCF developed a strategic approach, as the Moyen-Bafing National Park contains about 5000 chimpanzees as well as some 255 villages. Therefore, we adopted an "integrated landscape approach" whereby the community activities are planned in combination with initiatives increasing forest regeneration and connectivity in high conservation value areas. Communities in northern Guinea confronted with dramatic fluctuations due to climatic changes welcomed such activities that help them become more resilient and adaptable to those alterations. In conclusion, evidence-based information at the local level helps to resolve the conservation paradox by adapting with the local communities' context-specific dynamic approaches to enhance the conservation of great apes.

Systematic mapping of developmental milestones in wild chimpanzees.

Postnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one-species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter-individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d'Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter-individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development.

Environmental variability supports chimpanzee behavioural diversity.

Large brains and behavioural innovation are positively correlated, species-specific traits, associated with the behavioural flexibility animals need for adapting to seasonal and unpredictable habitats. Similar ecological challenges would have been important drivers throughout human evolution. However, studies examining the influence of environmental variability on within-species behavioural diversity are lacking despite the critical assumption that population diversification precedes genetic divergence and speciation. Here, using a dataset of 144 wild chimpanzee (Pan troglodytes) communities, we show that chimpanzees exhibit greater behavioural diversity in environments with more variability - in both recent and historical timescales. Notably, distance from Pleistocene forest refugia is associated with the presence of a larger number of behavioural traits, including both tool and non-tool use behaviours. Since more than half of the behaviours investigated are also likely to be cultural, we suggest that environmental variability was a critical evolutionary force promoting the behavioural, as well as cultural diversification of great apes.

Chimpanzees' technical reasoning: Taking fieldwork and ontogeny seriously.

Following the tradition of comparing humans with chimpanzees placed under unfavorable conditions, the authors suggest many uniquely human technological abilities. However, chimpanzees use spontaneously tools in nature to achieve many different goals demonstrating technological skills and reasoning contradicting the authors contrast. Chimpanzees and humans develop skills through the experiences faced during their upbringing and neglecting this leads to fake conclusions.

How isotopic signatures relate to meat consumption in wild chimpanzees: A critical reference study from Taï National Park, Côte d'Ivoire.

The roots of human hunting and meat eating lie deep in our evolutionary past shared with chimpanzees (Pan troglodytes). From the few habituated wild populations, we know that there is considerable variation in the extent to which chimpanzees consume meat. Expanding our knowledge of meat eating frequencies to more, yet unhabituated, populations requires noninvasive, indirect quantitative techniques. We here evaluate the use of stable isotopes to reconstruct meat-eating behavior in wild chimpanzees. We present hair isotope data (n = 260) of two western chimpanzee (P. troglodytes verus) groups from Taï forest (Côte d'Ivoire) and relate them to directly observed amounts of meat consumed, sex/female reproductive state, and group, while controlling for differences between individuals, seasons, and observation efforts. Succeeding seven months of hunting observations, we collected hair of 25 individuals for sequential analysis of δ15N and δ13C. Hunting success in the 7-month study period varied between the groups, with 25 successful hunts in the East group and only 8 in the North group. However, our models only found a direct relationship between amounts of meat consumed and variation within individual hair δ15N values in the East group, but not in the North group and not when comparing between individuals or groups. Although on average East group individuals consumed more than double the amount of meat than North group individuals, their δ15N values were significantly lower, suggesting that differences in microhabitat are substantial between group territories. The effect of sex/female reproductive state was significant in δ15N and δ13C, suggesting it related to access to food or feeding preferences. We conclude that several factors additional to diet are influencing and thus obscuring the isotope ratios in wild chimpanzee hair, particularly when comparing between sexes and social groups.

Author Correction: Chimpanzee ethnography reveals unexpected cultural diversity.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition.

Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The 'interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the 'social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.

Group dominance increases territory size and reduces neighbour pressure in wild chimpanzees.

Territorial social species, including humans, compete between groups over key resources. This between-group competition has evolutionary implications on adaptations like in-group cooperation even with non-kin. An emergent property of between-group competition is group dominance. Mechanisms of group dominance in wild animal populations are difficult to study, as they require long-term data on several groups within a population. Here, using long-term data on four neighbouring groups of wild western chimpanzees, we test the hypothesis that group dominance impacts the costs and benefits of between-group competition, measured by territory size and the pressure exerted by neighbouring groups. Larger groups had larger territories and suffered less neighbour pressure compared with smaller groups. Within-group increase in the number of males led to territory increase, suggesting the role of males in territory acquisition. However, variation in territory sizes and neighbour pressure was better explained by group size. This suggests that the bisexually-bonded social system of western chimpanzees, where females participate in territorial behaviour, confers a competitive advantage to larger groups and that group dominance acts through group size in this population. Considering variation in social systems offers new insights on how group dominance acts in territorial species and its evolutionary implications on within-group cooperation.

Chimpanzee ethnography reveals unexpected cultural diversity.

Human ethnographic knowledge covers hundreds of societies, whereas chimpanzee ethnography encompasses at most 15 communities. Using termite fishing as a window into the richness of chimpanzee cultural diversity, we address a potential sampling bias with 39 additional communities across Africa. Previously, termite fishing was known from eight locations with two distinguishable techniques observed in only two communities. Here, we add nine termite-fishing communities not studied before, revealing 38 different technical elements, as well as community-specific combinations of three to seven elements. Thirty of those were not ecologically constrained, permitting the investigation of chimpanzee termite-fishing culture. The number and combination of elements shared among individuals were more similar within communities than between them, thus supporting community-majority conformity via social imitation. The variation in community-specific combinations of elements parallels cultural diversity in human greeting norms or chopstick etiquette. We suggest that termite fishing in wild chimpanzees shows some elements of cumulative cultural diversity.