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.

A global risk assessment of primates under climate and land use/cover scenarios.

Primates are facing an impending extinction crisis, driven by extensive habitat loss, land use change and hunting. Climate change is an additional threat, which alone or in combination with other drivers, may severely impact those taxa unable to track suitable environmental conditions. Here, we investigate the extent of climate and land use/cover (LUC) change-related risks for primates. We employed an analytical approach to objectively select a subset of climate scenarios, for which we then calculated changes in climatic and LUC conditions for 2050 across primate ranges (N = 426 species) under a best-case scenario and a worst-case scenario. Generalized linear models were used to examine whether these changes varied according to region, conservation status, range extent and dominant habitat. Finally, we reclassified primate ranges based on different magnitudes of maximum temperature change, and quantified the proportion of ranges overall and of primate hotspots in particular that are likely to be exposed to extreme temperature increases. We found that, under the worst-case scenario, 74% of Neotropical forest-dwelling primates are likely to be exposed to maximum temperature increases up to 7°C. In contrast, 38% of Malagasy savanna primates will experience less pronounced warming of up to 3.5°C. About one quarter of Asian and African primates will face up to 50% crop expansion within their range. Primary land (undisturbed habitat) is expected to disappear across species' ranges, whereas secondary land (disturbed habitat) will increase by up to 98%. With 86% of primate ranges likely to be exposed to maximum temperature increases >3°C, primate hotspots in the Neotropics are expected to be particularly vulnerable. Our study highlights the fundamental exposure risk of a large percentage of primate ranges to predicted climate and LUC changes. Importantly, our findings underscore the urgency with which climate change mitigation measures need to be implemented to avert primate extinctions on an unprecedented scale.

Nocturnal activity in wild chimpanzees (Pan troglodytes): Evidence for flexible sleeping patterns and insights into human evolution.

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.

Phylogeny and species delimitations in European Dicranum (Dicranaceae, Bryophyta) inferred from nuclear and plastid DNA.

DNA sequences have been widely used for taxonomy, inferring phylogenetic relationships and identifying species boundaries. Several specific methods to define species delimitations based on molecular phylogenies have appeared recently, with the generalized mixed Yule coalescent (GMYC) method being most popular. However, only few studies on land plants have been published so far and GMYC analyses of bryophytes are missing. Dicranum is a large genus of mosses whose (morpho-)species are partly ill-defined and frequently confused. To infer molecular species delimitations, we reconstructed phylogenetic trees based on five chloroplast markers and nuclear ribosomal ITS sequences from 27 out of 30 species occurring in Europe. We applied the species delimitation methods GMYC and Poisson tree processes (PTP) in order to compare their discriminatory power with species boundaries inferred from the molecular phylogenetic reconstructions and with the morphological species concept. Phylogenetic circumscriptions were congruent with the morphological concept for 19 species, while eight species were molecularly not well delimited, mostly forming closely related species pairs. The automated species delimitation methods achieved similar results but tended to overestimate the number of potential species and exposed several incongruences between the morphological concept and inference from molecular phylogenetic reconstructions. It is concluded that GMYC and PTP methods potentially provide a useful and objective way of delimiting bryophyte species, but studies on further bryophyte data sets are necessary to infer whether incongruences might ensue from evolutionary processes and to test the suitability of these approaches.

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.

Phylogenetic relationship and molecular taxonomy of African grasses of the genus Panicum inferred from four chloroplast DNA-barcodes and nuclear gene sequences.

The genus Panicum s.l. comprises about 450 grass species in which the C4 and the C3 metabolic pathways of photosynthesis are realized. In the West African savannah, Panicum spp. and closely related taxa dominate the landscape, with species differentially adapted to drought conditions. We obtained four chloroplast DNA barcode sequences, rbcL, matK, ndhF and trnH-psbA intergenic region, for nine Panicum spp. with a focus on West African species, and we performed maximum likelihood analysis to infer their phylogenetic relationship. Furthermore the phylogenetic placement of five newly sequenced taxa was achieved using a published phylogeny of more than 300 Panicoids based on ndhF sequences. The comparison of the resulting phylogenetic tree constructed from a combination of all four barcode sequences with the one based on rbcL and matK showed that the latter combination of the two, is sufficient for the analysis. A tree constructed from amino acid sequences derived from isolated cDNAs of the nucleus-encoded phosphoenolpyruvate carboxylase displayed a similar topology. All ppc-sequences could be annotated to either ppc-B2 or ppc-aR. Moreover the inclusion of the West African Panicum species in an extensive dataset of Panicoids supports the proposition that within the subtribe Panicinae only the NAD-malic enzyme type of C4 photosynthesis is present.

Hunting of mammals by central chimpanzees (Pan troglodytes troglodytes) in the Loango National Park, Gabon.

The predation and consumption of animals are common behaviours in chimpanzees across tropical Africa. To date, however, relatively little is known concerning the hunting behaviour of central chimpanzees (Pan troglodytes troglodytes). Here, we provide the first direct observations of hunting behaviour by individuals of the newly habituated Rekambo community in the Loango National Park, Gabon. Over a period of 23 months (May 2017 to March 2019), we observed a total of 61 predation attempts on eight mammal species, including four monkey species. The two most frequently hunted species were two monkey species (Cercocebus torquatus, Cercopithecus nictitans), which are not hunted at other long-term field sites. The majority of predation events observed involved parties of an average of eight individuals, mainly adult males, with hunting success being higher with increasing numbers of participants. Hunting occurred all year round, but hunting rates increased in the dry season, the period of high fruit availability in the Loango National Park. These results are in line with the nutrient surplus hypothesis which explains seasonal variation in hunting behaviour in several populations of eastern chimpanzees (Pan troglodytes schweinfurthii: e.g., Mahale, Tanzania; Ngogo, Uganda). Finally, with a hunting frequency of 2.65 hunts per month, the Rekambo community had higher hunting rates than other sites (Bossou, Republic of Guinea; Kahuzi-Biega, Democratic Republic of Congo; Budongo, Uganda) where red colobus monkeys are also absent. We discuss these results and compare them to patterns at other long-term sites.

Structure of Chimpanzee Gut Microbiomes across Tropical Africa.

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.

Novelty Response of Wild African Apes to Camera Traps.

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.

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.

Which Latitudinal Gradients for Genetic Diversity?

A recent global analysis of GenBank DNA sequences from amphibians and mammals indicated consistent poleward decrease of intraspecific genetic diversity in both classes. We highlight that this result was biased by not accounting for distance decay of similarity and reanalyse the datasets, revealing distinct latitudinal gradients in mammals and amphibians.