Leprosy in wild chimpanzees.

Humans are considered as the main host for Mycobacterium leprae1, the aetiological agent of leprosy, but spillover has occurred to other mammals that are now maintenance hosts, such as nine-banded armadillos and red squirrels2,3. Although naturally acquired leprosy has also been described in captive nonhuman primates4-7, the exact origins of infection remain unclear. Here we describe leprosy-like lesions in two wild populations of western chimpanzees (Pan troglodytes verus) in Cantanhez National Park, Guinea-Bissau and Taï National Park, Côte d'Ivoire, West Africa. Longitudinal monitoring of both populations revealed the progression of disease symptoms compatible with advanced leprosy. Screening of faecal and necropsy samples confirmed the presence of M. leprae as the causative agent at each site and phylogenomic comparisons with other strains from humans and other animals show that the chimpanzee strains belong to different and rare genotypes (4N/O and 2F). These findings suggest that M. leprae may be circulating in more wild animals than suspected, either as a result of exposure to humans or other unknown environmental sources.

Automated detection of Bornean white-bearded gibbon (Hylobates albibarbis) vocalizations using an open-source framework for deep learning.

Passive acoustic monitoring is a promising tool for monitoring at-risk populations of vocal species, yet, extracting relevant information from large acoustic datasets can be time-consuming, creating a bottleneck at the point of analysis. To address this, an open-source framework for deep learning in bioacoustics to automatically detect Bornean white-bearded gibbon (Hylobates albibarbis) "great call" vocalizations in a long-term acoustic dataset from a rainforest location in Borneo is adapted. The steps involved in developing this solution are described, including collecting audio recordings, developing training and testing datasets, training neural network models, and evaluating model performance. The best model performed at a satisfactory level (F score = 0.87), identifying 98% of the highest-quality calls from 90 h of manually annotated audio recordings and greatly reduced analysis times when compared to a human observer. No significant difference was found in the temporal distribution of great call detections between the manual annotations and the model's output. Future work should seek to apply this model to long-term acoustic datasets to understand spatiotemporal variations in H. albibarbis' calling activity. Overall, a roadmap is presented for applying deep learning to identify the vocalizations of species of interest, which can be adapted for monitoring other endangered vocalizing species.

Seed dispersal syndrome predicts ethanol concentration of fruits in a tropical dry forest.

Studying fruit traits and their interactions with seed dispersers can improve how we interpret patterns of biodiversity, ecosystem function and evolution. Mounting evidence suggests that fruit ethanol is common and variable, and may exert selective pressures on seed dispersers. To test this, we comprehensively assess fruit ethanol content in a wild ecosystem and explore sources of variation. We hypothesize that both phylogeny and seed dispersal syndrome explain variation in ethanol levels, and we predict that fruits with mammalian dispersal traits will contain higher levels of ethanol than those with bird dispersal traits. We measured ripe fruit ethanol content in species with mammal- (n = 16), bird- (n = 14) or mixed-dispersal (n = 7) syndromes in a Costa Rican tropical dry forest. Seventy-eight per cent of fruit species yielded measurable ethanol concentrations. We detected a phylogenetic signal in maximum ethanol levels (Pagel's λ = 0.82). Controlling for phylogeny, we observed greater ethanol concentrations in mammal-dispersed fruits, indicating that dispersal syndrome helps explain variation in ethanol content, and that mammals may be more exposed to ethanol in their diets than birds. Our findings further our understanding of wild fruit ethanol and its potential role as a selective pressure on frugivore sensory systems and metabolism.

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.

Towards systematic and evidence-based conservation planning for western chimpanzees.

As animal populations continue to decline, frequently driven by large-scale land-use change, there is a critical need for improved environmental planning. While data-driven spatial planning is widely applied in conservation, as of yet it is rarely used for primates. The western chimpanzee (Pan troglodytes verus) declined by 80% within 24 years and was uplisted to Critically Endangered by the IUCN Red List of Threatened Species in 2016. To support conservation planning for western chimpanzees, we systematically identified geographic areas important for this taxon. We based our analysis on a previously published data set of modeled density distribution and on several scenarios that accounted for different spatial scales and conservation targets. Across all scenarios, typically less than one-third of areas we identified as important are currently designated as high-level protected areas (i.e., national park or IUCN category I or II). For example, in the scenario for protecting 50% of all chimpanzees remaining in West Africa (i.e., approximately 26,500 chimpanzees), an area of approximately 60,000 km2 was selected (i.e., approximately 12% of the geographic range), only 24% of which is currently designated as protected areas. The derived maps can be used to inform the geographic prioritization of conservation interventions, including protected area expansion, "no-go-zones" for industry and infrastructure, and conservation sites outside the protected area network. Environmental guidelines by major institutions funding infrastructure and resource extraction projects explicitly require corporations to minimize the negative impact on great apes. Therefore, our results can inform avoidance and mitigation measures during the planning phases of such projects. This study was designed to inform future stakeholder consultation processes that could ultimately integrate the conservation of western chimpanzees with national land-use priorities. Our approach may help in promoting similar work for other primate taxa to inform systematic conservation planning in times of growing threats.

Feeding ecology of chimpanzees (Pan troglodytes verus) inhabiting a forest-mangrove-savanna-agricultural matrix at Caiquene-Cadique, Cantanhez National Park, Guinea-Bissau.

With rising conversion of "natural" habitat to other land use such as agriculture, nonhuman primates are increasingly exploiting areas influenced by people and their activities. Despite the conservation importance of understanding the ways in which primates modify their behavior to human pressures, data are lacking, even for well-studied species. Using systematically collected data (fecal samples, feeding traces, and direct observations), we examined the diet and feeding strategies of an unhabituated chimpanzee community (Pan troglodytes verus) at Caiquene-Cadique in Guinea-Bissau that inhabit a forest-savanna-mangrove-agricultural mosaic. The chimpanzees experienced marked seasonal variations in the availability of plant foods, but maintained a high proportion of ripe fruit in the diet across months. Certain wild species were identified as important to this community including oil-palm (Elaeis guineensis) fruit and flower. Honey was frequently consumed but no other insects or vertebrates were confirmed to be eaten by this community. However, we provide indirect evidence of possible smashing and consumption of giant African snails (Achatina sp.) by chimpanzees at this site. Caiquene-Cadique chimpanzees were confirmed to feed on nine different agricultural crops, which represented 13.6% of all plant species consumed. Consumption of fruit and nonfruit crops was regular, but did not increase during periods of wild fruit scarcity. Crop consumption is an increasing and potentially problematic behavior, which can impact local people's tolerance toward wildlife. To maximize the potential success of any human-wildlife coexistence strategy (e.g., to reduce primate crop feeding), knowledge of primate behavior, as well as multifaceted social dimensions of interactions, is critical.

The evolutionary ecology of ethanol.

The consumption of ethanol has frequently been seen as largely restricted to humans. Here, we take a broad eco-evolutionary approach to understanding ethanol's potential impact on the natural world. There is growing evidence that ethanol is present in many wild fruits, saps, and nectars and that ethanol ingestion offers benefits that favour adaptations for its use in multiple taxa. Explanations for ethanol consumption span both the nutritional and non-nutritional, with potential medicinal value or cognitive effects (with social-behavioural benefits) explored. We conclude that ethanol is ecologically relevant and that it has shaped the evolution of many species and structured symbiotic relationships among organisms, including plants, yeast, bacteria, insects, and mammals.

Chimpanzees balance resources and risk in an anthropogenic landscape of fear.

Human-wildlife coexistence is possible when animals can meet their ecological requirements while managing human-induced risks. Understanding how wildlife balance these trade-offs in anthropogenic environments is crucial to develop effective strategies to reduce risks of negative interactions, including bi-directional aggression and disease transmission. For the first time, we use a landscape of fear framework with Bayesian spatiotemporal modelling to investigate anthropogenic risk-mitigation and optimal foraging trade-offs in Critically Endangered western chimpanzees (Pan troglodytes verus). Using 12 months of camera trap data (21 camera traps, 6722 camera trap days) and phenology on wild and cultivated plant species collected at Caiquene-Cadique, Cantanhez National Park (Guinea-Bissau), we show that humans and chimpanzees broadly overlapped in their use of forest and anthropogenic parts of the habitat including villages and cultivated areas. The spatiotemporal model showed that chimpanzee use of space was predicted by the availability of naturalised oil-palm fruit. Chimpanzees used areas away from villages and agriculture more intensively, but optimised their foraging strategies by increasing their use of village areas with cultivated fruits when wild fruits were scarce. Our modelling approach generates fine-resolution space-time output maps, which can be scaled-up to identify human-wildlife interaction hotspots at the landscape level, informing coexistence strategy.

Automated audiovisual behavior recognition in wild primates.

Large video datasets of wild animal behavior are crucial to produce longitudinal research and accelerate conservation efforts; however, large-scale behavior analyses continue to be severely constrained by time and resources. We present a deep convolutional neural network approach and fully automated pipeline to detect and track two audiovisually distinctive actions in wild chimpanzees: buttress drumming and nut cracking. Using camera trap and direct video recordings, we train action recognition models using audio and visual signatures of both behaviors, attaining high average precision (buttress drumming: 0.87 and nut cracking: 0.85), and demonstrate the potential for behavioral analysis using the automatically parsed video. Our approach produces the first automated audiovisual action recognition of wild primate behavior, setting a milestone for exploiting large datasets in ethology and conservation.

Envisioning a resilient future for biodiversity conservation in the wake of the COVID-19 pandemic.

As the COVID-19 pandemic continues to affect societies across the world, the ongoing economic and social disruptions are likely to present fundamental challenges for current and future biodiversity conservation.We review the literature for outcomes of past major societal, political, economic and zoonotic perturbations on biodiversity conservation, and demonstrate the complex implications of perturbation events upon conservation efforts. Building on the review findings, we use six in-depth case studies and the emerging literature to identify positive and negative outcomes of the COVID-19 pandemic, known and anticipated, for biodiversity conservation efforts around the world.A number of similarities exist between the current pandemic and past perturbations, with experiences highlighting that the pandemic-induced declines in conservation revenue and capacity, livelihood and trade disruptions are likely to have long-lasting and negative implications for biodiversity and conservation efforts.Yet, the COVID-19 pandemic also brought about a global pause in human movement that is unique in recent history, and may yet foster long-lasting behavioural and societal changes, presenting opportunities to strengthen and advance conservation efforts in the wake of the pandemic. Enhanced collaborations and partnerships at the local level, cross-sectoral engagement, local investment and leadership will all enhance the resilience of conservation efforts in the face of future perturbations. Other actions aimed at enhancing resilience will require fundamental institutional change and extensive government and public engagement and support if they are to be realised.The pandemic has highlighted the inherent vulnerabilities in the social and economic models upon which many conservation efforts are based. In so doing, it presents an opportunity to reconsider the status quo for conservation, and promotes behaviours and actions that are resilient to future perturbation. A free Plain Language Summary can be found within the Supporting Information of this article.

Flexible feeding on cultivated underground storage organs by rainforest-dwelling chimpanzees at Bossou, West Africa.

It has been proposed that exploitation of underground storage organs (USOs) played an important role in the evolution of the genus Homo, these items serving as 'fallback foods' during periods of low food availability. The use of USOs as food by wild chimpanzees is infrequent and seen mostly in populations inhabiting relatively arid environments, such as the savanna. Here, we specifically test the hypothesis that chimpanzees (Pan troglodytes verus) inhabiting tropical wet forest at Bossou (Republic of Guinea, West Africa) exploit USOs as a fallback food during periods of fruit scarcity. Chimpanzees were never observed feeding on wild USOs, that is, those that were never cultivated, and rarely on other underground plant parts. However, direct observations revealed regular consumption of the USOs of cultivated cassava (Manihot esculenta), a spatially abundant and continuously available plant, although the chimpanzees did not use tools when acquiring and feeding on cassava. In agreement with the fallback foods hypothesis, our results show that chimpanzees exploited cassava USOs more frequently when both wild and cultivated fruits were scarce, and consumption patterns of cassava paralleled those of wild fallback foods. These seasonal extractive USO foraging strategies by chimpanzees can strengthen attempts to construct a clearer picture of the importance of USO feeding in hominoid evolution.

The ethnoprimatological approach in primatology.

Recent and long-term sympatries between humans and nonhuman primates (hereafter primates) are central to the behavioral ecology, conservation, and evolutionary trajectories of numerous primate species. Ethnoprimatology emphasizes that interconnections between humans and primates should be viewed as more than just disruptions of a "natural" state, and instead anthropogenic contexts must be considered as potential drivers for specific primate behavioral patterns. Rather than focusing solely on the behavior and ecology of the primate species at hand, as in traditional primatology, or on the symbolic meanings and uses of primates, as in socio-cultural anthropology, ethnoprimatology attempts to merge these perspectives into a more integrative approach. As human pressures on environments continue to increase and primate habitats become smaller and more fragmented, the need for a primatology that considers the impact of human attitudes and behavior on all aspects of primate lives and survival is imperative. In this special issue, we present both data-driven examples and more general discussions that describe how ethnoprimatological approaches can be both a contribution to the core theory and practice of primatology and a powerful tool in our goal of conservation action.

Attacks on local persons by chimpanzees in Bossou, Republic of Guinea: long-term perspectives.

Attacks on humans by nonhuman primates are one of the most serious causes of human-primate conflict, and strongly influence people's perceptions and tolerance of nonhuman primates. Despite their importance, systematic and extensive records of such attacks are rare. Here, we report the attacks that occurred on local persons by chimpanzees (Pan troglodytes verus) at Bossou, Republic of Guinea, from 1995 to 2009. There have been a total of 11 attacks during this period, the majority of which were directed toward children. They varied in their severity, but all were nonfatal. Attacks took place on a road and narrow paths that bordered the forest or in cultivated fields and orchards where opportunities for human-chimpanzee contact are high. Attacks occurred between the months of March and October, coinciding with wild fruit scarcity, increased levels of crop-raiding, and periods of human cultivation with likely increased human usage of paths. Although the families of attack victims felt angry and fearful toward chimpanzees after attacks, some drew on their traditional beliefs to explain why chimpanzees were respected, protected, and could not hurt them, even when attacks occurred. We provide suggestions for reducing future nonhuman primate attacks on humans in an effort to mitigate human-primate conflict situations.

Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: feeding dynamics in a human-influenced environment.

Increased human population growth and more conversions of natural habitat to agricultural land have resulted in greater proximity between humans and nonhuman primate species. Consequent increases in resource competition including crop-raiding are a by-product of both natural resources becoming less available and the nutritional benefits of cultivated foods becoming more known to the nonhuman primates. Chimpanzees at Bossou in the Republic of Guinea, West Africa, consume 17 different types of cultivated foods that are grown extensively throughout their small, fragmented home range. Direct observations of feeding behavior conducted over an 18-month period revealed that during specific months crops account for up to one quarter of chimpanzee feeding time, with higher overall crop-raiding levels throughout the periods of wild fruit scarcity. Some cultivated foods, especially sugar fruits, are mostly fallback foods, whereas others, such as rice pith (Oryza sp.) and maize (Zea mays), are consumed according to their availability even when wild foods are abundant. These findings highlight the importance of both crop choice by farmers and a thorough understanding of the ecology of resident primate species when establishing land management techniques for alleviating human-primate conflict.

A comparison of methods to determine chimpanzee home-range size in a forest-farm mosaic at Madina in Cantanhez National Park, Guinea-Bissau.

Human activities impact the distribution of numerous species. Anthropogenic habitats are often fragmented, and wildlife must navigate through human-influenced and 'natural' parts of the landscape to access resources. Different methods to determine the home-range areas of nonhuman primates have not considered the additional complexities of ranging in anthropogenic areas. Here, using 6 months of spatial data on the distribution of chimpanzee presence (feces, feeding traces, nests, opportunistic encounters; n = 833) collected across the wet and dry seasons, we examine different analytical techniques to calculate the home-range size of an unhabituated chimpanzee (Pan troglodytes verus) community inhabiting a forest-farm mosaic at Madina, Cantanhez National Park in Guinea-Bissau. The minimum convex polygon method and the grid cell (500 m × 500 m cell size) method estimated the chimpanzees home-range size at 19.02 and 15.50 km2, respectively with kernel analysis calculating a lower value of 8.52 km2. For the grid cell method, home-range estimates varied with cell size, with larger cells producing larger estimates. We compare our home-range estimates with other chimpanzee research sites across Africa. We recommend the use of kernel analysis for determining primate home ranges, especially for those groups exploiting fragmented habitats including forest-farm mosaics, as this method takes account of inaccessible or infrequently used anthropogenic areas across the complete home range of the primate group. However, care must be taken when using this method, since it is sensitive to small sample sizes that can occur when studying unhabituated communities, resulting in underestimated home ranges.

Breaking Through Disciplinary Barriers: Human-Wildlife Interactions and Multispecies Ethnography.

One of the main challenges when integrating biological and social perspectives in primatology is overcoming interdisciplinary barriers. Unfamiliarity with subject-specific theory and language, distinct disciplinary-bound approaches to research, and academic boundaries aimed at "preserving the integrity" of subject disciplines can hinder developments in interdisciplinary research. With growing interest in how humans and other primates share landscapes, and recognition of the importance of combining biological and social information to do this effectively, the disparate use of terminology is becoming more evident. To tackle this problem, we dissect the meaning of what the biological sciences term studies in "human-wildlife conflict" or more recently "human-wildlife interactions" and compare it to what anthropology terms "multispecies ethnography." In the biological sciences, human-wildlife interactions are the actions resulting from people and wild animals sharing landscapes and resources, with outcomes ranging from being beneficial or harmful to one or both species. In the social sciences, human-nonhuman relationships have been explored on a philosophical, analytical, and empirical level. Building on previous work, we advocate viewing landscapes through an interdisciplinary "multispecies lens" in which humans are observed as one of multiple organisms that interact with other species to shape and create environments. To illustrate these interconnections we use the case study of coexistence between people of the Nalu ethnic group and Critically Endangered western chimpanzees (Pan troglodytes verus) at Cantanhez National Park in Guinea-Bissau, to demonstrate how biological and social research approaches can be complementary and can inform conservation initiatives at the human-primate interface. Finally, we discuss how combining perspectives from ethnoprimatology with those from multispecies ethnography can advance the study of ethnoprimatology to aid productive discourse and enhance future interdisciplinary research.

Placentophagy in wild chimpanzees (Pan troglodytes verus) at Bossou, Guinea.

Despite intensive observation of nonhuman great apes during long-term field studies, observations of great ape births in the wild are rare. Research on wild chimpanzees (Pan troglodytes verus) at Bossou in the Republic of Guinea has been ongoing for 35 years, yet chimpanzee parturitions have been observed on only two occasions. Here we provide information regarding both chimpanzee births, with detailed information from the close observation of one. During this birth, the mother built a day nest in a tree before parturition. After giving birth, the mother consumed the placenta, and the other chimpanzees in her party gathered near her and her neonate. However, she did not share the placenta, and consumed it all herself. In the second observation, the mother also built a nest in a tree and subsequently gave birth. Thereafter, she shared the placenta with some individuals and consumed part of the placenta herself. Although maternal placentophagy is a ubiquitous behavior among the majority of non-human primates, observations of placenta sharing by wild primates are infrequent, and the proximate and ultimate explanations for the behavior remain unclear.

Tailored Enrichment Strategies and Stereotypic Behavior in Captive Individually Housed Macaques (Macaca spp.).

The welfare of nonhuman animals in captivity is widely dependent on the natural psychological, physical, and behavioral needs of the animals and how adequately these needs are met. Inability to engage in natural behaviors can lead to chronic stress and expression of stereotypic behavior. The majority of research on decreasing stereotypic behavior in captivity addresses problems at the group level and does not account for individual variability in each animal's needs, history, and preferences. This study combined physiological and behavioral measures of well being to comprehensively assess the unique needs of individually housed captive macaques (Macaca spp.) with the aim of developing tailored welfare strategies. Behavioral and hormonal data were collected under 2 conditions: baseline and individualized enrichment. The results showed a significant decrease in stereotypic behavior under the enrichment condition. Additionally, 7 out of 9 individuals showed a decrease in fecal glucocorticoid (stress hormone) levels, indicating a reduction in hypothalamic-pituitary-adrenal activity. Addressing welfare on an individual, rather than group, level allows for a better overall characterization of well being and maximizes the probability of improving the welfare of each animal.

Tools to tipple: ethanol ingestion by wild chimpanzees using leaf-sponges.

African apes and humans share a genetic mutation that enables them to effectively metabolize ethanol. However, voluntary ethanol consumption in this evolutionary radiation is documented only in modern humans. Here, we report evidence of the long-term and recurrent ingestion of ethanol from the raffia palm (Raphia hookeri, Arecaceae) by wild chimpanzees (Pan troglodytes verus) at Bossou in Guinea, West Africa, from 1995 to 2012. Chimpanzees at Bossou ingest this alcoholic beverage, often in large quantities, despite an average presence of ethanol of 3.1% alcohol by volume (ABV) and up to 6.9% ABV. Local people tap raffia palms and the sap collects in plastic containers, and chimpanzees use elementary technology-a leafy tool-to obtain this fermenting sap. These data show that ethanol does not act as a deterrent to feeding in this community of wild apes, supporting the idea that the last common ancestor of living African apes and modern humans was not averse to ingesting foods containing ethanol.

Apes in the Anthropocene: flexibility and survival.

We are in a new epoch, the Anthropocene, and research into our closest living relatives, the great apes, must keep pace with the rate that our species is driving change. While a goal of many studies is to understand how great apes behave in natural contexts, the impact of human activities must increasingly be taken into account. This is both a challenge and an opportunity, which can importantly inform research in three diverse fields: cognition, human evolution, and conservation. No long-term great ape research site is wholly unaffected by human influence, but research at those that are especially affected by human activity is particularly important for ensuring that our great ape kin survive the Anthropocene.