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.

Global importance of Indigenous Peoples, their lands, and knowledge systems for saving the world's primates from extinction.

Primates, represented by 521 species, are distributed across 91 countries primarily in the Neotropic, Afrotropic, and Indo-Malayan realms. Primates inhabit a wide range of habitats and play critical roles in sustaining healthy ecosystems that benefit human and nonhuman communities. Approximately 68% of primate species are threatened with extinction because of global pressures to convert their habitats for agricultural production and the extraction of natural resources. Here, we review the scientific literature and conduct a spatial analysis to assess the significance of Indigenous Peoples' lands in safeguarding primate biodiversity. We found that Indigenous Peoples' lands account for 30% of the primate range, and 71% of primate species inhabit these lands. As their range on these lands increases, primate species are less likely to be classified as threatened or have declining populations. Safeguarding Indigenous Peoples' lands, languages, and cultures represents our greatest chance to prevent the extinction of the world's primates.

Inter-community behavioural variation confirmed through indirect methods in four neighbouring chimpanzee communities in Cantanhez NP, Guinea-Bissau.

Culture, while long viewed as exclusively human, has now been demonstrated across diverse taxa and contexts. However, most animal culture data are constrained to well-studied, habituated groups. This is the case for chimpanzees, arguably the most 'cultural' non-human species. While much progress has been made charting wild chimpanzees' cultural repertoire, large gaps remain in our knowledge of the majority of the continent's chimpanzees. Furthermore, few studies have compared neighbouring communities, despite such comparisons providing the strongest evidence for culture, and few have studied communities living in anthropogenic habitats although their culture is in imminent danger of disappearing. Here we combine direct, indirect and remote methods, including camera traps, to study, over 2 years, four unhabituated neighbouring chimpanzee communities inhabiting human-impacted habitats in Cantanhez NP, Guinea-Bissau. From traces collected during 1089 km of reconnaissance walks and 4197 videos from 56 camera trap locations, we identified 18 putative cultural traits. These included some noteworthy novel behaviours for these communities, and behaviours possibly new to the species. We created preliminary behavioural profiles for each community, and found inter-community differences spanning tool use, communication, and social behaviour, demonstrating the importance of comparing neighbouring communities and of studying previously neglected communities including those inhabiting anthropogenic landscapes.

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.

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.

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.

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.

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.

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.

Primate occurrence across a human-impacted landscape in Guinea-Bissau and neighbouring regions in West Africa: using a systematic literature review to highlight the next conservation steps.

BACKGROUND: West African landscapes are largely characterised by complex agroforest mosaics. Although the West African forests are considered a nonhuman primate hotspot, knowledge on the distribution of many species is often lacking and out-of-date. Considering the fast-changing nature of the landscapes in this region, up-to-date information on primate occurrence is urgently needed, particularly of taxa such as colobines, which may be more sensitive to habitat modification than others. Understanding wildlife occurrence and mechanisms of persistence in these human-dominated landscapes is fundamental for developing effective conservation strategies. METHODS: In this paper, we aim to review current knowledge on the distribution of three threatened primates in Guinea-Bissau and neighbouring regions, highlighting research gaps and identifying priority research and conservation action. We conducted a systematic literature review of primate studies from 1976 to 2016 in Guinea-Bissau, southern Senegal and western Guinea (Boké Region). We mapped historical observation records of chimpanzee (Pan troglodytes verus), Temminck's red colobus (Pilicolobus badius temminckii) and king colobus (Colobus polykomos), including our preliminary survey data from Dulombi, a newly established National Park (NP) in Guinea-Bissau. RESULTS: We found 151 documents, including 87 journal articles, that contained field data on primates in this region. In Guinea-Bissau, nearly all studies focussed south of the Corubal River, including mainly Cantanhez, Cufada, and Boé NP's. In Senegal, most of the data came from Fongoli and Niokolo-Koba NP. In Boké (Guinea) studies are few, with the most recent data coming from Sangarédi. In Dulombi NP we recorded eight primate species, including chimpanzees, red colobus and king colobus. Across the selected region, chimpanzees, red colobus and king colobus were reported in eleven, twelve and seven protected areas, respectively. DISCUSSION: Our study demonstrates large geographical research gaps particularly for the two colobines. For the first time after more than two decades, we confirm the presence of red colobus and king colobus north of the Corubal River in Guinea-Bissau. The little information available from large parts of the red colobus range raises questions regarding levels of population fragmentation in this species, particularly in Casamance and across northern Guinea-Bissau. There are still no records demonstrating the occurrence of king colobus in Senegal, and the presence of a viable population in north-eastern Guinea-Bissau remains uncertain. While the occurrence of chimpanzees in Guinea-Bissau and Senegal is well documented, data from Boké (Guinea) are sparse and out-of-date. Our approach-the mapping of data gathered from a systematic literature review-allows us to provide recommendations for selecting future geographical survey locations and planning further research and conservation strategies in this region.

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.

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.

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.

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.

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.

Wild chimpanzees show group differences in selection of agricultural crops.

The ability of wild animals to respond flexibly to anthropogenic environmental changes, including agriculture, is critical to survival in human-impacted habitats. Understanding use of human foods by wildlife can shed light on the acquisition of novel feeding habits and how animals respond to human-driven land-use changes. Little attention has focused on within-species variation in use of human foods or its causes. We examined crop-feeding in two groups of wild chimpanzees - a specialist frugivore - with differing histories of exposure to agriculture. Both groups exploited a variety of crops, with more accessible crops consumed most frequently. However, crop selection by chimpanzees with long-term exposure to agriculture was more omnivorous (i.e., less fruit-biased) compared to those with more recent exposure, which ignored most non-fruit crops. Our results suggest chimpanzees show increased foraging adaptations to cultivated landscapes over time; however, local feeding traditions may also contribute to group differences in crop-feeding in this species. Understanding the dynamic responses of wildlife to agriculture can help predict current and future adaptability of species to fast-changing anthropogenic landscapes.