Many morphs: Parsing gesture signals from the noise.

Parsing signals from noise is a general problem for signallers and recipients, and for researchers studying communicative systems. Substantial efforts have been invested in comparing how other species encode information and meaning, and how signalling is structured. However, research depends on identifying and discriminating signals that represent meaningful units of analysis. Early approaches to defining signal repertoires applied top-down approaches, classifying cases into predefined signal types. Recently, more labour-intensive methods have taken a bottom-up approach describing detailed features of each signal and clustering cases based on patterns of similarity in multi-dimensional feature-space that were previously undetectable. Nevertheless, it remains essential to assess whether the resulting repertoires are composed of relevant units from the perspective of the species using them, and redefining repertoires when additional data become available. In this paper we provide a framework that takes data from the largest set of wild chimpanzee (Pan troglodytes) gestures currently available, splitting gesture types at a fine scale based on modifying features of gesture expression using latent class analysis (a model-based cluster detection algorithm for categorical variables), and then determining whether this splitting process reduces uncertainty about the goal or community of the gesture. Our method allows different features of interest to be incorporated into the splitting process, providing substantial future flexibility across, for example, species, populations, and levels of signal granularity. Doing so, we provide a powerful tool allowing researchers interested in gestural communication to establish repertoires of relevant units for subsequent analyses within and between systems of communication.

A case of suspected chimpanzee scavenging in the Issa Valley, Tanzania.

Like humans, chimpanzees (Pan troglodytes) are well known for their vertebrate and invertebrate hunting, but they rarely scavenge. In contrast, while hunting and meat consumption became increasingly important during the evolution of the genus Homo, scavenging meat and marrow from carcasses of large mammals was also likely to be an important component of their subsistence strategies. Here, we describe a confrontational scavenging interaction between an adult male chimpanzee from the Issa Valley and a crowned eagle (Stephanoaetus coronatus), which resulted in the chimpanzee capturing and consuming the carcass of a juvenile bushbuck (Tragelaphus scriptus). We describe the interaction and contextualize this with previous scavenging observations from chimpanzees.

A case of intercommunity lethal aggression by chimpanzees in an open and dry landscape, Issa Valley, western Tanzania.

Intercommunity (lethal) aggression is a familiar component of the behavioural repertoire of many forest-dwelling chimpanzee (Pan troglodytes) communities. However, until now, the absence of intercommunity attacks - including killings - in communities that live in open, mosaic environments has supported hypotheses of reduced resource competition in drier habitats, and informed referential models of early hominin social dynamics in a similar habitat. In June 2020, we observed the first instance of intercommunity lethal aggression, a male-committed infanticide, by the Issa chimpanzee community, which live in a savannah-mosaic habitat in the Issa Valley, western Tanzania. The carcass was recovered by researchers after it was abandoned by the attackers. Here, we give a detailed account of the events leading up to and including the infanticide, and contextualise our observations with what has been described for other chimpanzee communities. Notably, in contrast to the majority of reported intercommunity infanticides, the infant male victim was castrated (and not cannibalised), making this the youngest reported castration. This observation of intercommunity aggression disproves its hypothesised absence in savannah-dwelling chimpanzees, which by extension, has implications for early hominin evolution. We suggest that the near absence of observations of intercommunity aggression in savannah chimpanzee communities is most likely due to the lack of long-term study communities, and in some cases geographic isolation. We hypothesise that food-rich areas within a habitat with otherwise widely distributed food sources may select for intense intercommunity aggression despite the low population density characteristic of savannah communities. Anecdotes such as this add to the comparative database available on intercommunity killings in chimpanzee society, improving our ability to draw inferences about their evolutionary significance.

Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species.

Wild chimpanzee behavior suggests that a savanna-mosaic habitat did not support the emergence of hominin terrestrial bipedalism.

Bipedalism, a defining feature of the human lineage, is thought to have evolved as forests retreated in the late Miocene-Pliocene. Chimpanzees living in analogous habitats to early hominins offer a unique opportunity to investigate the ecological drivers of bipedalism that cannot be addressed via the fossil record alone. We investigated positional behavior and terrestriality in a savanna-mosaic community of chimpanzees (Pan troglodytes schweinfurthii) in the Issa Valley, Tanzania as the first test in a living ape of the hypothesis that wooded, savanna habitats were a catalyst for terrestrial bipedalism. Contrary to widely accepted hypotheses of increased terrestriality selecting for habitual bipedalism, results indicate that trees remained an essential component of the hominin adaptive niche, with bipedalism evolving in an arboreal context, likely driven by foraging strategy.

The ecology and epidemiology of malaria parasitism in wild chimpanzee reservoirs.

Chimpanzees (Pan troglodytes) harbor rich assemblages of malaria parasites, including three species closely related to P. falciparum (sub-genus Laverania), the most malignant human malaria parasite. Here, we characterize the ecology and epidemiology of malaria infection in wild chimpanzee reservoirs. We used molecular assays to screen chimpanzee fecal samples, collected longitudinally and cross-sectionally from wild populations, for malaria parasite mitochondrial DNA. We found that chimpanzee malaria parasitism has an early age of onset and varies seasonally in prevalence. A subset of samples revealed Hepatocystis mitochondrial DNA, with phylogenetic analyses suggesting that Hepatocystis appears to cross species barriers more easily than Laverania. Longitudinal and cross-sectional sampling independently support the hypothesis that mean ambient temperature drives spatiotemporal variation in chimpanzee Laverania infection. Infection probability peaked at ~24.5 °C, consistent with the empirical transmission optimum of P. falciparum in humans. Forest cover was also positively correlated with spatial variation in Laverania prevalence, consistent with the observation that forest-dwelling Anophelines are the primary vectors. Extrapolating these relationships across equatorial Africa, we map spatiotemporal variation in the suitability of chimpanzee habitat for Laverania transmission, offering a hypothetical baseline indicator of human exposure risk.

Spatio-temporal changes in chimpanzee density and abundance in the Greater Mahale Ecosystem, Tanzania.

Species conservation and management require reliable information about animal distribution and population size. Better management actions within a species' range can be achieved by identifying the location and timing of population changes. In the Greater Mahale Ecosystem (GME), western Tanzania, deforestation due to the expansion of human settlements and agriculture, annual burning, and logging are known threats to wildlife. For one of the most charismatic species, the endangered eastern chimpanzee (Pan troglodytes schweinfurthii), approximately 75% of the individuals are distributed outside national park boundaries, requiring monitoring and protection efforts over a vast landscape of various protection statuses. These efforts are especially challenging when we lack data on trends in density and population size. To predict spatio-temporal chimpanzee density and abundance across the GME, we used density surface modeling, fitting a generalized additive model to a 10-year time-series data set of nest counts based on line-transect surveys. The chimpanzee population declined at an annual rate of 2.41%, including declines of 1.72% in riparian forests (from this point forward, forests), 2.05% in miombo woodlands (from this point forward, woodlands) and 3.45% in nonforests. These population declines were accompanied by ecosystem-wide declines in vegetation types of 1.36% and 0.32% per year for forests and woodlands, respectively; we estimated an annual increase of 1.35% for nonforests. Our model predicted the highest chimpanzee density in forests (0.86 chimpanzees/km2 , 95% confidence intervals (CIs) 0.60-1.23; as of 2020), followed by woodlands (0.19, 95% CI 0.12-0.30) and nonforests (0.18, 95% CI 0.10-1.33). Although forests represent only 6% of the landscape, they support nearly one-quarter of the chimpanzee population (769 chimpanzees, 95% CI 536-1103). Woodlands dominate the landscape (71%) and therefore support more than a half of the chimpanzee population (2294; 95% CI 1420-3707). The remaining quarter of the landscape is represented by nonforests and supports another quarter of the chimpanzee population (750; 95% CI 408-1381). Given the pressures on the remaining suitable habitat in Tanzania, and the need of chimpanzees to access both forest and woodland vegetation to survive, we urge future management actions to increase resources and expand the efforts to protect critical forest and woodland habitat and promote strategies and policies that more effectively prevent irreversible losses. We suggest that regular monitoring programs implement a systematic random design to effectively inform and allocate conservation actions and facilitate interannual comparisons for trend monitoring, measuring conservation success, and guiding adaptive management.

Understanding External Influences on Target Detection and Classification Using Camera Trap Images and Machine Learning.

Using machine learning (ML) to automate camera trap (CT) image processing is advantageous for time-sensitive applications. However, little is currently known about the factors influencing such processing. Here, we evaluate the influence of occlusion, distance, vegetation type, size class, height, subject orientation towards the CT, species, time-of-day, colour, and analyst performance on wildlife/human detection and classification in CT images from western Tanzania. Additionally, we compared the detection and classification performance of analyst and ML approaches. We obtained wildlife data through pre-existing CT images and human data using voluntary participants for CT experiments. We evaluated the analyst and ML approaches at the detection and classification level. Factors such as distance and occlusion, coupled with increased vegetation density, present the most significant effect on DP and CC. Overall, the results indicate a significantly higher detection probability (DP), 81.1%, and correct classification (CC) of 76.6% for the analyst approach when compared to ML which detected 41.1% and classified 47.5% of wildlife within CT images. However, both methods presented similar probabilities for daylight CT images, 69.4% (ML) and 71.8% (analysts), and dusk CT images, 17.6% (ML) and 16.2% (analysts), when detecting humans. Given that users carefully follow provided recommendations, we expect DP and CC to increase. In turn, the ML approach to CT image processing would be an excellent provision to support time-sensitive threat monitoring for biodiversity conservation.

Localizing wild chimpanzees with passive acoustics.

Localizing wildlife contributes in multiple ways to species conservation. Data on animal locations can reveal elements of social behavior, habitat use, population dynamics, and be useful in calculating population density. Acoustic localization systems (ALS) are a non-invasive method widely used in the marine sciences but not well established and rarely employed for terrestrial species.We deployed an acoustic array in a mountainous environment with heterogeneous vegetation, comprised of four custom-built GPS synchronized acoustic sensors at about 500 m intervals in Issa Valley, western Tanzania, covering an area of nearly 2 km2. Our goal was to assess the precision and error of the estimated locations by conducting playback tests, but also by comparing the estimated locations of wild chimpanzee calls with their true locations obtained in parallel during follows of individual chimpanzees. We assessed the factors influencing localization error, such as wind speed and temperature, which fluctuate during the day and are known to affect sound transmission.We localized 282 playback sounds and found that the mean localization error was 27 ± 21.8 m. Localization was less prone to error and more precise during early mornings (6:30 h) compared to other periods. We further localized 22 wild chimpanzee loud calls within 52 m of the location of a researcher closely following the calling individuals.We demonstrate that acoustic localization is a powerful tool for chimpanzee monitoring, with multiple behavioral and conservation applications. Its applicability in studying social dynamics and revealing density estimation among many others, especially but not exclusively for loud calling species, provides an efficient way of monitoring populations and informing conservation plans to mediate species loss.

Association of human disturbance and gastrointestinal parasite infection of yellow baboons in western Tanzania.

Human disturbance is an ongoing threat to many wildlife species, manifesting as habitat destruction, resource overuse, or increased disease exposure, among others. With increasing human: non-human primate (NHP) encounters, NHPs are increasingly susceptible to human-introduced diseases, including those with parasitic origins. As such, epidemiology of parasitic disease is becoming an important consideration for NHP conservation strategies. To investigate the relationship between parasite infections and human disturbance we studied yellow baboons (Papio cynocephalus) living outside of national park boundaries in western Tanzania, collecting 135 fresh faecal samples from nine troops occupying areas with varying levels of human disturbance. We fixed all samples in 10% formalin and later evaluated parasite prevalence and abundance (of isotrichid ciliates and Strongylida). We identified seven protozoan and four helminth taxa. Taxa showed varied relationships with human disturbance, baboon troop size and host age. In four taxa, we found a positive association between prevalence and troop size. We also report a trend towards higher parasite prevalence of two taxa in less disturbed areas. To the contrary, high levels of human disturbance predicted increased abundance of isotrichid ciliates, although no relationship was found between disturbance and Strongylida abundance. Our results provide mixed evidence that human disturbance is associated with NHP parasite infections, highlighting the need to consider monitoring parasite infections when developing NHP conservation strategies.

Chimpanzee (Pan troglodytes schweinfurthii) grouping patterns in an open and dry savanna landscape, Issa Valley, western Tanzania.

Fission-fusion societies are social systems in which individuals belonging to the same community are rarely all together but rather spend most of their time in temporary parties. This flexible social organization is assumed to be an adaptation that balances advantages and costs of group living in a fluid way as resources and constraints shift through space and time. It has been argued that this flexibility freed hominins from the foraging constraints caused by living in large groups. Given their close genetic relationship to humans and because they represent the classic case of a fission-fusion society, chimpanzees have often been used as referential models to understand human social evolution. Determinants of chimpanzee party size have been widely studied for decades across several communities. However, we lack data from open and dry sites-which closely resemble those reconstructed for Plio-Pleistocene hominins-on communities that potentially face similar environmental constraints as early hominins did. We investigated chimpanzee (Pan troglodytes schweinfurthii) grouping patterns on a recently habituated community living in the savanna-woodland mosaic landscape of the Issa Valley, western Tanzania, by following chimpanzees daily and recording party size every hour. Our results revealed that party size at Issa 1) followed seasonal fluctuations in food availability, 2) increased in the presence of swollen females, and 3) was higher in open vegetation, which potentially presents a high predation risk. Furthermore, we found the Issa community to be highly cohesive compared with the majority of other communities, possibly due to a combination of its small size and potential threats characterizing its home range. Our study fills a gap in our knowledge of chimpanzee sociality by exploring grouping pattern determinants in an East African understudied biome and highlights what elements of early hominin social behavior may have evolved in Late Pliocene landscapes.

Vocal communication in wild chimpanzees: a call rate study.

BACKGROUND: Patterns of vocal communication have implications for species conservation: a change in calling behaviour can, for instance, reflect a disturbed habitat. More importantly, call rate is a parameter that allows conservation planners to convert call density into animal density, when detecting calls with a passive acoustic monitoring system (PAM). METHODS: We investigated chimpanzee (Pan troglodytes schweinfurthii) call rate during the late dry season in the Issa Valley, western Tanzania by conducting focal follows. We examined the socio-ecological factors that influence call production rate of savanna woodland chimpanzees. RESULTS: We found that sex, proportion of time spent in a vegetation type, proportion of time spent travelling, time of the day, party size and swollen parous female presence had a significant effect on the call rate. Call rate differed among the different demographic classes with subadult and adult males vocalising twice as often as the subadult and adult females and three times as often as the juveniles. APPLICATIONS: The use of PAM and recent statistical developments to estimate animal density is promising but relies on our knowing individual call rate, often not available for many species. With the improvement in automatic call detection, we anticipate that PAM will increasingly be broadly applied to primates but also across taxa, for conservation.

Chimpanzees (Pan troglodytes) in savanna landscapes.

Chimpanzees (Pan troglodytes) are the only great apes that inhabit hot, dry, and open savannas. We review the environmental pressures of savannas on chimpanzees, such as food and water scarcity, and the evidence for chimpanzees' behavioral responses to these landscapes. In our analysis, savannas were generally associated with low chimpanzee population densities and large home ranges. In addition, thermoregulatory behaviors that likely reduce hyperthermia risk, such as cave use, were frequently observed in the hottest and driest savanna landscapes. We hypothesize that such responses are evidence of a "savanna landscape effect" in chimpanzees and offer pathways for future research to understand its evolutionary processes and mechanisms. We conclude by discussing the significance of research on savanna chimpanzees to modeling the evolution of early hominin traits and informing conservation programs for these endangered apes.

An Evaluation of the Factors Affecting 'Poacher' Detection with Drones and the Efficacy of Machine-Learning for Detection.

Drones are being increasingly used in conservation to tackle the illegal poaching of animals. An important aspect of using drones for this purpose is establishing the technological and the environmental factors that increase the chances of success when detecting poachers. Recent studies focused on investigating these factors, and this research builds upon this as well as exploring the efficacy of machine-learning for automated detection. In an experimental setting with voluntary test subjects, various factors were tested for their effect on detection probability: camera type (visible spectrum, RGB, and thermal infrared, TIR), time of day, camera angle, canopy density, and walking/stationary test subjects. The drone footage was analysed both manually by volunteers and through automated detection software. A generalised linear model with a logit link function was used to statistically analyse the data for both types of analysis. The findings concluded that using a TIR camera improved detection probability, particularly at dawn and with a 90° camera angle. An oblique angle was more effective during RGB flights, and walking/stationary test subjects did not influence detection with both cameras. Probability of detection decreased with increasing vegetation cover. Machine-learning software had a successful detection probability of 0.558, however, it produced nearly five times more false positives than manual analysis. Manual analysis, however, produced 2.5 times more false negatives than automated detection. Despite manual analysis producing more true positive detections than automated detection in this study, the automated software gives promising, successful results, and the advantages of automated methods over manual analysis make it a promising tool with the potential to be successfully incorporated into anti-poaching strategies.

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.

Correction: Ecological correlates of chimpanzee (Pan troglodytes schweinfurthii) density in Mahale Mountains National Park, Tanzania.

[This corrects the article DOI: 10.1371/journal.pone.0246628.].

CD4 receptor diversity represents an ancient protection mechanism against primate lentiviruses.

Infection with human and simian immunodeficiency viruses (HIV/SIV) requires binding of the viral envelope glycoprotein (Env) to the host protein CD4 on the surface of immune cells. Although invariant in humans, the Env binding domain of the chimpanzee CD4 is highly polymorphic, with nine coding variants circulating in wild populations. Here, we show that within-species CD4 diversity is not unique to chimpanzees but found in many African primate species. Characterizing the outermost (D1) domain of the CD4 protein in over 500 monkeys and apes, we found polymorphic residues in 24 of 29 primate species, with as many as 11 different coding variants identified within a single species. D1 domain amino acid replacements affected SIV Env-mediated cell entry in a single-round infection assay, restricting infection in a strain- and allele-specific fashion. Several identical CD4 polymorphisms, including the addition of N-linked glycosylation sites, were found in primate species from different genera, providing striking examples of parallel evolution. Moreover, seven different guenons (Cercopithecus spp.) shared multiple distinct D1 domain variants, pointing to long-term trans-specific polymorphism. These data indicate that the HIV/SIV Env binding region of the primate CD4 protein is highly variable, both within and between species, and suggest that this diversity has been maintained by balancing selection for millions of years, at least in part to confer protection against primate lentiviruses. Although long-term SIV-infected species have evolved specific mechanisms to avoid disease progression, primate lentiviruses are intrinsically pathogenic and have left their mark on the host genome.

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.