Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest.

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

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.

Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

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.

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

The Critically Endangered western chimpanzee declines by 80.

African large mammals are under extreme pressure from unsustainable hunting and habitat loss. Certain traits make large mammals particularly vulnerable. These include late age at first reproduction, long inter-birth intervals, and low population density. Great apes are a prime example of such vulnerability, exhibiting all of these traits. Here we assess the rate of population change for the western chimpanzee, Pan troglodytes verus, over a 24-year period. As a proxy for change in abundance, we used transect nest count data from 20 different sites archived in the IUCN SSC A.P.E.S. database, representing 25,000 of the estimated remaining 35,000 western chimpanzees. For each of the 20 sites, datasets for 2 different years were available. We estimated site-specific and global population change using Generalized Linear Models. At 12 of these sites, we detected a significant negative trend. The estimated change in the subspecies abundance, as approximated by nest encounter rate, yielded a 6% annual decline and a total decline of 80.2% over the study period from 1990 to 2014. This also resulted in a reduced geographic range of 20% (657,600 vs. 524,100 km2 ). Poverty, civil conflict, disease pandemics, agriculture, extractive industries, infrastructure development, and lack of law enforcement, are some of the many reasons for the magnitude of threat. Our status update triggered the uplisting of the western chimpanzee to "Critically Endangered" on the IUCN Red List. In 2017, IUCN will start updating the 2003 Action Plan for western chimpanzees and will provide a consensus blueprint for what is needed to save this subspecies. We make a plea for greater commitment to conservation in West Africa across sectors. Needed especially is more robust engagement by national governments, integration of conservation priorities into the private sector and development planning across the region and sustained financial support from donors.

Threat of mining to African great apes.

The rapid growth of clean energy technologies is driving a rising demand for critical minerals. In 2022 at the 15th Conference of the Parties to the Convention on Biological Diversity (COP15), seven major economies formed an alliance to enhance the sustainability of mining these essential decarbonization minerals. However, there is a scarcity of studies assessing the threat of mining to global biodiversity. By integrating a global mining dataset with great ape density distribution, we estimated the number of African great apes that spatially coincided with industrial mining projects. We show that up to one-third of Africa's great ape population faces mining-related risks. In West Africa in particular, numerous mining areas overlap with fragmented ape habitats, often in high-density ape regions. For 97% of mining areas, no ape survey data are available, underscoring the importance of increased accessibility to environmental data within the mining sector to facilitate research into the complex interactions between mining, climate, biodiversity, and sustainability.

Local genetic adaptation to habitat in wild chimpanzees.

How populations adapt to their environment is a fundamental question in biology. Yet we know surprisingly little about this process, especially for endangered species such as non-human great apes. Chimpanzees, our closest living relatives, are particularly interesting because they inhabit diverse habitats, from rainforest to woodland-savannah. Whether genetic adaptation facilitates such habitat diversity remains unknown, despite having wide implications for evolutionary biology and conservation. Using 828 newly generated exomes from wild chimpanzees, we find evidence of fine-scale genetic adaptation to habitat. Notably, adaptation to malaria in forest chimpanzees is mediated by the same genes underlying adaptation to malaria in humans. This work demonstrates the power of non-invasive samples to reveal genetic adaptations in endangered populations and highlights the importance of adaptive genetic diversity for chimpanzees.

Population dynamics and genetic connectivity in recent chimpanzee history.

Knowledge on the population history of endangered species is critical for conservation, but whole-genome data on chimpanzees (Pan troglodytes) is geographically sparse. Here, we produced the first non-invasive geolocalized catalog of genomic diversity by capturing chromosome 21 from 828 non-invasive samples collected at 48 sampling sites across Africa. The four recognized subspecies show clear genetic differentiation correlating with known barriers, while previously undescribed genetic exchange suggests that these have been permeable on a local scale. We obtained a detailed reconstruction of population stratification and fine-scale patterns of isolation, migration, and connectivity, including a comprehensive picture of admixture with bonobos (Pan paniscus). Unlike humans, chimpanzees did not experience extended episodes of long-distance migrations, which might have limited cultural transmission. Finally, based on local rare variation, we implement a fine-grained geolocalization approach demonstrating improved precision in determining the origin of confiscated chimpanzees.

Recent genetic connectivity and clinal variation in chimpanzees.

Much like humans, chimpanzees occupy diverse habitats and exhibit extensive behavioural variability. However, chimpanzees are recognized as a discontinuous species, with four subspecies separated by historical geographic barriers. Nevertheless, their range-wide degree of genetic connectivity remains poorly resolved, mainly due to sampling limitations. By analyzing a geographically comprehensive sample set amplified at microsatellite markers that inform recent population history, we found that isolation by distance explains most of the range-wide genetic structure of chimpanzees. Furthermore, we did not identify spatial discontinuities corresponding with the recognized subspecies, suggesting that some of the subspecies-delineating geographic barriers were recently permeable to gene flow. Substantial range-wide genetic connectivity is consistent with the hypothesis that behavioural flexibility is a salient driver of chimpanzee responses to changing environmental conditions. Finally, our observation of strong local differentiation associated with recent anthropogenic pressures portends future loss of critical genetic diversity if habitat fragmentation and population isolation continue unabated.

Geographically structured genomic diversity of non-human primate-infecting Treponema pallidum subsp. pertenue.

Many non-human primate species in sub-Saharan Africa are infected with Treponema pallidum subsp. pertenue, the bacterium causing yaws in humans. In humans, yaws is often characterized by lesions of the extremities and face, while T. pallidum subsp. pallidum causes venereal syphilis and is typically characterized by primary lesions on the genital, anal or oral mucosae. It remains unclear whether other T. pallidum subspecies found in humans also occur in non-human primates and how the genomic diversity of non-human primate T. pallidum subsp. pertenue lineages is distributed across hosts and space. We observed orofacial and genital lesions in sooty mangabeys (Cercocebus atys) in Taï National Park, Côte d'Ivoire and collected swabs and biopsies from symptomatic animals. We also collected non-human primate bones from 8 species in Taï National Park and 16 species from 11 other sites across sub-Saharan Africa. Samples were screened for T. pallidum DNA using polymerase chain reactions (PCRs) and we used in-solution hybridization capture to sequence T. pallidum genomes. We generated three nearly complete T. pallidum genomes from biopsies and swabs and detected treponemal DNA in bones of six non-human primate species in five countries, allowing us to reconstruct three partial genomes. Phylogenomic analyses revealed that both orofacial and genital lesions in sooty mangabeys from Taï National Park were caused by T. pallidum subsp. pertenue. We showed that T. pallidum subsp. pertenue has infected non-human primates in Taï National Park for at least 28 years and has been present in two non-human primate species that had not been described as T. pallidum subsp. pertenue hosts in this ecosystem, western chimpanzees (Pan troglodytes verus) and western red colobus (Piliocolobus badius), complementing clinical evidence that started accumulating in Taï National Park in 2014. More broadly, simian T. pallidum subsp. pertenue strains did not form monophyletic clades based on host species or the symptoms caused, but rather clustered based on geography. Geographical clustering of T. pallidum subsp. pertenue genomes might be compatible with cross-species transmission of T. pallidum subsp. pertenue within ecosystems or environmental exposure, leading to the acquisition of closely related strains. Finally, we found no evidence for mutations that confer antimicrobial resistance.

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.

Human impact erodes chimpanzee behavioral diversity.

Chimpanzees possess a large number of behavioral and cultural traits among nonhuman species. The "disturbance hypothesis" predicts that human impact depletes resources and disrupts social learning processes necessary for behavioral and cultural transmission. We used a dataset of 144 chimpanzee communities, with information on 31 behaviors, to show that chimpanzees inhabiting areas with high human impact have a mean probability of occurrence reduced by 88%, across all behaviors, compared to low-impact areas. This behavioral diversity loss was evident irrespective of the grouping or categorization of behaviors. Therefore, human impact may not only be associated with the loss of populations and genetic diversity, but also affects how animals behave. Our results support the view that "culturally significant units" should be integrated into wildlife conservation.

The impact of the Ebola virus disease (EVD) epidemic on agricultural production and livelihoods in Liberia.

There is unequivocal evidence in the literature that epidemics adversely affect the livelihoods of individuals, households and communities. However, evidence in the literature is dominated by the socioeconomic impacts of HIV/AIDS and malaria, while evidence on the impact of the Ebola virus disease (EVD) on households' livelihoods remains fragmented and scant. Our study investigates the effect of the EVD epidemic on the livelihoods of Liberian households using the Sustainable Livelihood Framework (SLF). The study also explores the effect of the EVD epidemic on agricultural production and productive efficiency of farm households using Spatial Stochastic Frontier Analysis (SSFA). We collected data from 623 households across Liberia in 2015, using a systematic random sampling design. Our results indicated that the annual income of sample households from communities where EVD occurred did not differ from the annual income of households from communities where EVD did not occur. Nonetheless, the majority of sample households reported a decrease in their income, compared to their income in the year before the survey. This suggests that the impact of the EVD epidemic might not only have been limited to communities directly affected by the epidemic, but also it may have indirectly affected communities in areas where EVD was not reported. We also found that the community-level incidence of EVD negatively affected crop production of farm households, which may have exacerbated the problem of food insecurity throughout the country. Moreover, we found that the EVD epidemic weakened the society's trust in Liberian institutions. In a nutshell, our results highlight that epidemics, such as the recent EVD outbreak, may have long-lasting negative effects on the livelihoods of a society and their effect may extend beyond the communities directly affected by the epidemics. This means that the nation's recovery from the impact of the epidemic would be more challenging, and the social and economic impacts of the epidemic may extend well beyond the end of the health crisis.

The socio-economic drivers of bushmeat consumption during the West African Ebola crisis.

Bushmeat represents an important source of animal protein for humans in tropical Africa. Unsustainable bushmeat hunting is a major threat to wildlife and its consumption is associated with an increased risk of acquiring zoonotic diseases, such as Ebola virus disease (EVD). During the recent EVD outbreak in West Africa, it is likely that human dietary behavior and local attitudes toward bushmeat consumption changed in response to the crisis, and that the rate of change depended on prevailing socio-economic conditions, including wealth and education. In this study, we therefore investigated the effects of income, education, and literacy on changes in bushmeat consumption during the crisis, as well as complementary changes in daily meal frequency, food diversity and bushmeat preference. More specifically, we tested whether wealthier households with more educated household heads decreased their consumption of bushmeat during the EVD crisis, and whether their daily meal frequency and food diversity remained constant. We used Generalized Linear Mixed Models to analyze interview data from two nationwide household surveys across Liberia. We found an overall decrease in bushmeat consumption during the crisis across all income levels. However, the rate of bushmeat consumption in high-income households decreased less than in low-income households. Daily meal frequency decreased during the crisis, and the diversity of food items and preferences for bushmeat species remained constant. Our multidisciplinary approach to study the impact of EVD can be applied to assess how other disasters affect social-ecological systems and improve our understanding and the management of future crises.

Chimpanzee accumulative stone throwing.

The study of the archaeological remains of fossil hominins must rely on reconstructions to elucidate the behaviour that may have resulted in particular stone tools and their accumulation. Comparatively, stone tool use among living primates has illuminated behaviours that are also amenable to archaeological examination, permitting direct observations of the behaviour leading to artefacts and their assemblages to be incorporated. Here, we describe newly discovered stone tool-use behaviour and stone accumulation sites in wild chimpanzees reminiscent of human cairns. In addition to data from 17 mid- to long-term chimpanzee research sites, we sampled a further 34 Pan troglodytes communities. We found four populations in West Africa where chimpanzees habitually bang and throw rocks against trees, or toss them into tree cavities, resulting in conspicuous stone accumulations at these sites. This represents the first record of repeated observations of individual chimpanzees exhibiting stone tool use for a purpose other than extractive foraging at what appear to be targeted trees. The ritualized behavioural display and collection of artefacts at particular locations observed in chimpanzee accumulative stone throwing may have implications for the inferences that can be drawn from archaeological stone assemblages and the origins of ritual sites.