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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.
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Doenças dos Animais/mortalidade , Animais Selvagens/microbiologia , Antraz/veterinária , Bacillus anthracis/patogenicidade , Mamíferos/microbiologia , Floresta Úmida , Clima Tropical , África Subsaariana , Doenças dos Animais/microbiologia , Animais , Antraz/microbiologia , Antraz/mortalidade , Bacillus anthracis/isolamento & purificação , Dípteros/microbiologia , Extinção Biológica , Feminino , Masculino , Pan troglodytes/microbiologia , Parques Recreativos , FilogeniaRESUMO
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.
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Pan troglodytes , Refúgio de Vida Selvagem , Animais , Biodiversidade , Clima , Ecossistema , Variação Genética , FilogeografiaRESUMO
OBJECTIVES: We investigated occurrences and patterns of terrestrial nocturnal activity in wild chimpanzees (Pan troglodytes) and modelled the influence of various ecological predictors on nocturnal activity. METHODS: Data were extracted from terrestrial camera-trap footage and ecological surveys from 22 chimpanzee study sites participating in the Pan African Programme: The Cultured Chimpanzee. We described videos demonstrating nocturnal activity, and we tested the effects of the percentage of forest, abundance of predators (lions, leopards and hyenas), abundance of large mammals (buffalos and elephants), average daily temperature, rainfall, human activity, and percent illumination on the probability of nocturnal activity. RESULTS: We found terrestrial nocturnal activity to occur at 18 of the 22 study sites, at an overall average proportion of 1.80% of total chimpanzee activity, and to occur during all hours of the night, but more frequently during twilight hours. We found a higher probability of nocturnal activity with lower levels of human activity, higher average daily temperature, and at sites with a larger percentage of forest. We found no effect of the abundance of predators and large mammals, rainfall, or moon illumination. DISCUSSION: Chimpanzee terrestrial nocturnal activity appears widespread yet infrequent, which suggests a consolidated sleeping pattern. Nocturnal activity may be driven by the stress of high daily temperatures and may be enabled at low levels of human activity. Human activity may exert a relatively greater influence on chimpanzee nocturnal behavior than predator presence. We suggest that chimpanzee nocturnal activity is flexible, enabling them to respond to changing environmental factors.
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Comportamento Animal/fisiologia , Pan troglodytes/fisiologia , Sono/fisiologia , Vigília/fisiologia , Animais , Antropologia Física , Evolução Biológica , Ecossistema , Humanos , TemperaturaRESUMO
Wild chimpanzees regularly use tools, made from sticks, leaves, or stone, to find flexible solutions to the ecological challenges of their environment. Nevertheless, some studies suggest strong limitations in the tool-using capabilities of chimpanzees. In this context, we present the discovery of a newly observed tool-use behavior in a population of chimpanzees (Pan troglodytes verus) living in the Bakoun Classified Forest, Guinea, where a temporary research site was established for 15 months. Bakoun chimpanzees of every age-sex class were observed to fish for freshwater green algae, Spirogrya sp., from rivers, streams, and ponds using long sticks and twigs, ranging from 9 cm up to 4.31 m in length. Using remote camera trap footage from 11 different algae fishing sites within an 85-km2 study area, we found that algae fishing occurred frequently during the dry season and was non-existent during the rainy season. Chimpanzees were observed algae fishing for as little as 1 min to just over an hour, with an average duration of 9.09 min. We estimate that 364 g of Spirogyra algae could be retrieved in this time, based on human trials in the field. Only one other chimpanzee population living in Bossou, Guinea, has been described to customarily scoop algae from the surface of the water using primarily herbaceous tools. Here, we describe the new behavior found at Bakoun and compare it to the algae scooping observed in Bossou chimpanzees and the occasional variant reported in Odzala, Republic of the Congo. As these algae are reported to be high in protein, carbohydrates, and minerals, we hypothesize that chimpanzees are obtaining a nutritional benefit from this seasonally available resource.
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Comportamento Alimentar , Pan troglodytes , Comportamento de Utilização de Ferramentas , Animais , Congo , Guiné , Microalgas , Estações do AnoRESUMO
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.
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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.
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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.
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Isótopos de Carbono/análise , Comportamento Alimentar/fisiologia , Isópteros/metabolismo , África , Animais , Comportamento Animal/fisiologia , Carbono/metabolismo , Dieta , Ecologia , Florestas , Pradaria , Isópteros/química , Nitrogênio/metabolismo , Isótopos de Nitrogênio/análise , Pan troglodytes/metabolismo , PlantasRESUMO
Noninvasive samples as a source of DNA are gaining interest in genomic studies of endangered species. However, their complex nature and low endogenous DNA content hamper the recovery of good quality data. Target capture has become a productive method to enrich the endogenous fraction of noninvasive samples, such as faeces, but its sensitivity has not yet been extensively studied. Coping with faecal samples with an endogenous DNA content below 1% is a common problem when prior selection of samples from a large collection is not possible. However, samples classified as unfavourable for target capture sequencing might be the only representatives of unique specific geographical locations, or to answer the question of interest. To explore how library complexity may be increased without repeating DNA extractions and generating new libraries, in this study we captured the exome of 60 chimpanzees (Pan troglodytes) using faecal samples with very low proportions of endogenous content (<1%). Our results indicate that by performing additional hybridizations of the same libraries, the molecular complexity can be maintained to achieve higher coverage. Also, whenever possible, the starting DNA material for capture should be increased. Finally, we specifically calculated the sequencing effort needed to avoid exhausting the library complexity of enriched faecal samples with low endogenous DNA content. This study provides guidelines, schemes and tools for laboratories facing the challenges of working with noninvasive samples containing extremely low amounts of endogenous DNA.
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Exoma , Genômica , Hibridização de Ácido Nucleico , Animais , Fezes , Biblioteca Gênica , Sequenciamento de Nucleotídeos em Larga Escala , Pan troglodytes/genética , Análise de Sequência de DNARESUMO
Understanding variation in host-associated microbial communities is important given the relevance of microbiomes to host physiology and health. Using 560 fecal samples collected from wild chimpanzees (Pan troglodytes) across their range, we assessed how geography, genetics, climate, vegetation, and diet relate to gut microbial community structure (prokaryotes, eukaryotic parasites) at multiple spatial scales. We observed a high degree of regional specificity in the microbiome composition, which was associated with host genetics, available plant foods, and potentially with cultural differences in tool use, which affect diet. Genetic differences drove community composition at large scales, while vegetation and potentially tool use drove within-region differences, likely due to their influence on diet. Unlike industrialized human populations in the United States, where regional differences in the gut microbiome are undetectable, chimpanzee gut microbiomes are far more variable across space, suggesting that technological developments have decoupled humans from their local environments, obscuring regional differences that could have been important during human evolution. IMPORTANCE Gut microbial communities are drivers of primate physiology and health, but the factors that influence the gut microbiome in wild primate populations remain largely undetermined. We report data from a continent-wide survey of wild chimpanzee gut microbiota and highlight the effects of genetics, vegetation, and potentially even tool use at different spatial scales on the chimpanzee gut microbiome, including bacteria, archaea, and eukaryotic parasites. Microbial community dissimilarity was strongly correlated with chimpanzee population genetic dissimilarity, and vegetation composition and consumption of algae, honey, nuts, and termites were potentially associated with additional divergence in microbial communities between sampling sites. Our results suggest that host genetics, geography, and climate play a far stronger role in structuring the gut microbiome in chimpanzees than in humans.
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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.
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Comportamento Animal , Evolução Molecular , Variação Genética , Componentes Genômicos , Repetições de Microssatélites , Pan troglodytes/genética , Migração Animal , Animais , Ecossistema , Interação Gene-Ambiente , Genética Populacional , Pan troglodytes/psicologia , Filogenia , Especificidade da EspécieRESUMO
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.
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Cercocebus atys/microbiologia , Genoma Bacteriano/genética , Doenças dos Macacos/transmissão , Treponema/genética , Bouba/veterinária , Animais , Côte d'Ivoire , Sequenciamento de Nucleotídeos em Larga Escala , Doenças dos Macacos/microbiologia , Reação em Cadeia da Polimerase , Treponema/isolamento & purificação , Sequenciamento Completo do Genoma , Bouba/microbiologia , Bouba/transmissãoRESUMO
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.
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Comportamento Animal , Pan troglodytes/psicologia , Animais , Ecossistema , Meio Ambiente , Feminino , Florestas , Masculino , Pan troglodytes/fisiologia , Comportamento de Utilização de FerramentasRESUMO
Herpesviruses are thought to have evolved in very close association with their hosts. This is notably the case for cytomegaloviruses (CMVs; genus Cytomegalovirus) infecting primates, which exhibit a strong signal of co-divergence with their hosts. Some herpesviruses are however known to have crossed species barriers. Based on a limited sampling of CMV diversity in the hominine (African great ape and human) lineage, we hypothesized that chimpanzees and gorillas might have mutually exchanged CMVs in the past. Here, we performed a comprehensive molecular screening of all 9 African great ape species/subspecies, using 675 fecal samples collected from wild animals. We identified CMVs in eight species/subspecies, notably generating the first CMV sequences from bonobos. We used this extended dataset to test competing hypotheses with various degrees of co-divergence/number of host switches while simultaneously estimating the dates of these events in a Bayesian framework. The model best supported by the data involved the transmission of a gorilla CMV to the panine (chimpanzee and bonobo) lineage and the transmission of a panine CMV to the gorilla lineage prior to the divergence of chimpanzees and bonobos, more than 800,000 years ago. Panine CMVs then co-diverged with their hosts. These results add to a growing body of evidence suggesting that viruses with a double-stranded DNA genome (including other herpesviruses, adenoviruses, and papillomaviruses) often jumped between hominine lineages over the last few million years.
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Temperament and personality research in humans and nonhuman animals measures behavioral variation in individual, population, or species-specific traits with implications for survival and fitness, such as social status, foraging, and mating success [1-5]. Curiosity and risk-taking tendencies have been studied extensively across taxa by measuring boldness and exploration responses to experimental novelty exposure [3, 4, 6-15]. Here, we conduct a natural field experiment using wildlife monitoring technology to test variation in the reaction of wild great apes (43 groups of naive chimpanzees, bonobos, and western gorillas across 14 field sites in Africa) to a novel object, the camera trap. Bonobo and gorilla groups demonstrated a stronger looking impulse toward the camera trap device compared to chimpanzees, suggesting higher visual attention and curiosity. Bonobos were also more likely to show alarm and other fearful behaviors, although such neophobic (and conversely, neophilic) responses were generally rare. Among all three species, individuals looked at cameras longer when they were young, were associating with fewer individuals, and did not live near a long-term research site. Overall, these findings partially validate results from great ape novelty paradigms in captivity [7, 8]. We further suggest that species-typical leadership styles [16] and social and environmental effects, including familiarity with humans, best explain novelty responses of wild great apes. In sum, this study illustrates the feasibility of large-scale field experiments and the importance of both intrinsic and extrinsic factors in shaping animal curiosity. VIDEO ABSTRACT.
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Comportamento Exploratório , Gorilla gorilla/psicologia , Pan paniscus/psicologia , Pan troglodytes/psicologia , Fotografação/instrumentação , África , Animais , Feminino , Masculino , Especificidade da EspécieRESUMO
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.
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Conservação dos Recursos Naturais/métodos , Pan troglodytes/psicologia , Comportamento Social , Animais , Conjuntos de Dados como Assunto , HumanosRESUMO
We present a range-wide assessment of sympatric western lowland gorillas Gorilla gorilla gorilla and central chimpanzees Pan troglodytes troglodytes using the largest survey data set ever assembled for these taxa: 59 sites in five countries surveyed between 2003 and 2013, totaling 61,000 person-days of fieldwork. We used spatial modeling to investigate major drivers of great ape distribution and population trends. We predicted density across each taxon's geographic range, allowing us to estimate overall abundance: 361,900 gorillas and 128,700 chimpanzees in Western Equatorial Africa-substantially higher than previous estimates. These two subspecies represent close to 99% of all gorillas and one-third of all chimpanzees. Annual population decline of gorillas was estimated at 2.7%, maintaining them as Critically Endangered on the International Union for Conservation of Nature and Natural Resources (IUCN) Red List. We quantified the threats to each taxon, of which the three greatest were poaching, disease, and habitat degradation. Gorillas and chimpanzees are found at higher densities where forest is intact, wildlife laws are enforced, human influence is low, and disease impacts have been low. Strategic use of the results of these analyses could conserve the majority of gorillas and chimpanzees. With around 80% of both subspecies occurring outside protected areas, their conservation requires reinforcement of anti-poaching efforts both inside and outside protected areas (particularly where habitat quality is high and human impact is low), diligent disease control measures (including training, advocacy, and research into Ebola virus disease), and the preservation of high-quality habitat through integrated land-use planning and implementation of best practices by the extractive and agricultural industries.
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Armas de Fogo , Gorilla gorilla , Pan troglodytes , Árvores , África , Animais , Geografia , Modelos Teóricos , Densidade Demográfica , Dinâmica PopulacionalRESUMO
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.
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Comportamento Animal , Pan troglodytes , África Ocidental , Animais , GeografiaRESUMO
Hunting is one of the main driving forces behind large mammal density distribution in many regions of the world. In tropical Africa, urban demand for bushmeat has been shown to dominate over subsistence hunting and its impact often overrides spatial-ecological species characteristics. To effectively protect remaining mammal populations the main factors that influence their distribution need to be integrated into conservation area prioritisation and management plans. This information has been lacking for Río Muni, Equatorial Guinea, as prior studies have been outdated or have not systematically covered the continental region of the country. In this study we evaluated: 1) the relative importance of local vs. commercial hunting; 2) wildlife density of protected vs. non-protected areas; and 3) the importance of ecological factors vs. human influence in driving mammal density distribution in Río Muni. We adopted a systematic countrywide line transect approach with particular focus on apes and elephants, but also including other mammal species. For analysis of field data we used generalised linear models with a set of predictor variables representing ecological conditions, anthropogenic pressure and protected areas. We estimate that there are currently 884 (437-1,789) elephants and 11,097 (8,719-13,592) chimpanzees and gorillas remaining in Río Muni. The results indicate strong hunting pressures on both local and commercial levels, with roads demonstrating a negative impact on elephants and overall mammal body mass. Protected areas played no role in determining any of the mammal species distributions and significant human hunting signs were found inside these protected areas, illustrating the lack of environmental law enforcement throughout the country. Río Muni is currently under-represented in conservation efforts in Western Equatorial Africa, and we recommend a focus on cross-boundary conservation, in particular in the Monte Alén-Monts de Cristal and Río Campo Ma'an conservation landscapes, where the highest densities and diversity of large mammals remain.