Socioecological factors influencing intraspecific variation in ranging dynamics of western lowland gorillas (Gorilla gorilla gorilla) in Ndoki Forest.

Ranging dynamics are physical and behavioral representations of how different socioecological factors affect an organism's spatial decisions and space use strategies. Western lowland gorillas (Gorilla gorilla gorilla) are a model species to investigate the drivers of spatial dynamics based on both the natural variation in socioecological factors within the species and compared with their mountain gorilla counterparts. In this study, we evaluate the influences of resource seasonality and social dynamics on variation in home range size, utilization, and intergroup overlap among multiple gorilla groups over an 8-year study period in the northern Republic of Congo. This study shows that western lowland gorillas can have small home ranges comparable to mountain gorillas, rather than universally larger home ranges as previously supposed, and that home ranges are stable through time. The largest source of variation in space use was the degree of intergroup home range overlap. The study groups did not demonstrate intraspecific variation in range size nor changes in intergroup overlap with respect to seasonality of fruit resources, but all groups demonstrated expansion of monthly range and core area with group size, matching predictions of intragroup feeding competition. These findings highlight the potential impact of intergroup relationships on space use and prompt further research on the role of social dynamics in ranging strategies. In this study, we reveal a greater degree of variability and flexibility in gorilla ranging behavior than previously realized which is relevant to improving comparative studies and informing conservation strategies on behalf of these endangered primates.

Planning abilities of wild chimpanzees (Pan troglodytes troglodytes) in tool-using contexts.

Planning is a type of problem solving in which a course of future action is devised via mental computation. Potential advantages of planning for tool use include reduced effort to gather tools, closer alignment to an efficient tool design, and increased foraging efficiency. Chimpanzees (Pan troglodytes troglodytes) in the Goualougo Triangle use a variety of different types of tools. We hypothesized that procurement strategy (brought to the termite nest, manufactured or acquired at the termite nest, or borrowed from others) reflects planning for current needs, with tool transport behavior varying by tool type and by age and sex class. It is also possible that chimpanzees anticipate the need for tools at future times, which would be evidenced by transporting multiple tool types for a sequential task. One year of video recordings at termite nests were systematically screened for tool procurement; data comprised 299 tool procurement events across 66 chimpanzees. In addition, we screened video recordings of leaf sponging and honey gathering, which resulted in another 38 procurement events. Fishing probes, which are typically used during a single visit, were typically transported to termite nests, while puncturing tools, which are durable and remain on site, were more often acquired at termite nests. Most tools transported in multiples were fishing probes, perhaps in anticipation that a single probe might not last through an entire foraging bout or might be transferred to another chimpanzee. We further documented that chimpanzees transported tool sets, comprising multiple different tool types used in sequence. Mature chimpanzees transported tools more often than did immatures. These observations suggest that chimpanzees plan tool use flexibly, reflecting the availability of raw materials and the likelihood that specific tool types will be needed for particular tasks. Developmental studies and further integration of behavioral, spatial, and archaeological data will help to illuminate the decision making and time depth of planning associated with tool technologies in living primates and hominin ancestors.

Path To Acceptance and Refined Practices for Habituating Western Lowland Gorillas.

Although western lowland gorillas (Gorilla gorilla gorilla) are the most numerous and widespread gorilla subspecies, they have remained relatively unstudied. International tourism has been initiated at several sites in the Congo Basin, which necessitates habituation of gorillas to human presence. However, habituation has proven difficult due to several obstacles, including relatively low population densities, small group sizes, and thick understory vegetation. In this article, we propose refinements to current approaches to habituating western lowland gorillas that maximize safety and emphasize adaptive responses based on empirical evidence. In addition to reviewing published reports, our approach is informed by the recent habituation of the Mététélé group in the Djéké Triangle, an area that was recently included in the Nouabalé-Ndoki National Park in Republic of Congo. We evaluate progress in habituation according to time spent in the presence of the gorillas and their reactions to humans. The Mététélé group is composed of 14 individuals and has a home range that overlaps with two habituated gorilla groups. Early in the habituation process, we discovered that three of Mététélé's group members were individuals who had previously been habituated as members of other groups. The presence of these individuals expedited the habituation process. Familiarity with humans may have also reduced aggressive responses during the habituation process. The overall result is a refined step-by-step approach to the habituation of western lowland gorillas that includes procedures and assessments to meet best-practice guidelines and ensure the wellbeing of both gorillas and humans.

Extending the conservation impact of great ape research: Flagship species sites facilitate biodiversity assessments and land preservation.

To inform regional conservation planning, we assessed mammalian and avian biodiversity in the Djéké Triangle, which is an intact forest with long-term research and tourism focused on western lowland gorillas (Gorilla gorilla gorilla). This critical region serves as a conservation conduit between the Nouabalé-Ndoki National Park (NNNP) in the Republic of Congo and the Dzanga-Ndoki National Park in Central African Republic. Wildlife inventories were conducted to determine if biodiversity in the Djéké Triangle (initially part of a logging concession) was equivalent to the NNNP. Camera traps (CTs) were deployed to estimate species richness, relative abundance, naïve occupancy, and activity patterns of medium-to-large species in mixed species and monodominant Gilbertiodendron forests that comprise the majority of regional terra firma. Species inventories were collected from CTs positioned on a grid and at termite nests throughout the Djéké Triangle and compared to CTs placed in the Goualougo Triangle located within the NNNP. From 10,534 camera days at 65 locations, we identified 34 mammal and 16 bird species. Allaying concerns of wildlife depletion, metrics of species richness in the Djéké Triangle surpassed those of the Goualougo Triangle. Many species were observed to occur across habitats, while others showed habitat specificity, with termite mounds indicated as an important microhabitat feature. Our comparisons of animal activity budgets in different habitat types provide important reference information for other populations and contexts. In conclusion, this study provided empirical evidence of the high conservation value of this region that contributed to increasing the protected status of the Djéké Triangle.

Widespread extinctions of co-diversified primate gut bacterial symbionts from humans.

Humans and other primates harbour complex gut bacterial communities that influence health and disease, but the evolutionary histories of these symbioses remain unclear. This is partly due to limited information about the microbiota of ancestral primates. Here, using phylogenetic analyses of metagenome-assembled genomes (MAGs), we show that hundreds of gut bacterial clades diversified in parallel (that is, co-diversified) with primate species over millions of years, but that humans have experienced widespread losses of these ancestral symbionts. Analyses of 9,460 human and non-human primate MAGs, including newly generated MAGs from chimpanzees and bonobos, revealed significant co-diversification within ten gut bacterial phyla, including Firmicutes, Actinobacteriota and Bacteroidota. Strikingly, ~44% of the co-diversifying clades detected in African apes were absent from available metagenomic data from humans and ~54% were absent from industrialized human populations. In contrast, only ~3% of non-co-diversifying clades detected in African apes were absent from humans. Co-diversifying clades present in both humans and chimpanzees displayed consistent genomic signatures of natural selection between the two host species but differed in functional content from co-diversifying clades lost from humans, consistent with selection against certain functions. This study discovers host-species-specific bacterial symbionts that predate hominid diversification, many of which have undergone accelerated extinctions from human populations.

Malaria-driven adaptation of MHC class I in wild bonobo populations.

The malaria parasite Plasmodium falciparum causes substantial human mortality, primarily in equatorial Africa. Enriched in affected African populations, the B*53 variant of HLA-B, a cell surface protein that presents peptide antigens to cytotoxic lymphocytes, confers protection against severe malaria. Gorilla, chimpanzee, and bonobo are humans' closest living relatives. These African apes have HLA-B orthologs and are infected by parasites in the same subgenus (Laverania) as P. falciparum, but the consequences of these infections are unclear. Laverania parasites infect bonobos (Pan paniscus) at only one (TL2) of many sites sampled across their range. TL2 spans the Lomami River and has genetically divergent subpopulations of bonobos on each side. Papa-B, the bonobo ortholog of HLA-B, includes variants having a B*53-like (B07) peptide-binding supertype profile. Here we show that B07 Papa-B occur at high frequency in TL2 bonobos and that malaria appears to have independently selected for different B07 alleles in the two subpopulations.

Predictors of respiratory illness in western lowland gorillas.

Infectious disease is hypothesized to be one of the most important causes of morbidity and mortality in wild great apes. Specific socioecological factors have been shown to influence incidences of respiratory illness and disease prevalence in some primate populations. In this study, we evaluated potential predictors (including age, sex, group size, fruit availability, and rainfall) of respiratory illness across three western lowland gorilla groups in the Republic of Congo. A total of 19,319 observational health assessments were conducted during daily follows of habituated gorillas in the Goualougo and Djéké Triangles over a 4-year study period. We detected 1146 incidences of clinical respiratory signs, which indicated the timing of probable disease outbreaks within and between groups. Overall, we found that males were more likely to exhibit signs than females, and increasing age resulted in a higher likelihood of respiratory signs. Silverback males showed the highest average monthly prevalence of coughs and sneezes (Goualougo: silverback Loya, 9.35 signs/month; Djéké: silverback Buka, 2.65 signs/month; silverback Kingo,1.88 signs/month) in each of their groups. Periods of low fruit availability were associated with an increased likelihood of respiratory signs. The global pandemic has increased awareness about the importance of continuous monitoring and preparedness for infectious disease outbreaks, which are also known to threaten wild ape populations. In addition to the strict implementation of disease prevention protocols at field sites focused on great apes, there is a need for heightened vigilance and systematic monitoring across sites to protect both wildlife and human populations.

Portrayals of wild primates in documentary films: reason for concern?

Documentaries are the primary means by which many people observe the behavior of wild primates. By influencing layperson perceptions of wild primates, documentaries could impact viewer conservation-related beliefs and behaviors and, therefore, the well-being of wild primates. To investigate such portrayals, we examined documentaries depicting the four species that were most represented in documentaries: rhesus macaque, chimpanzee, ring-tailed lemur, and mountain gorilla. For each documentary, we continuously coded behavior, conducted scan samples of age-sex classes at 3-min intervals, and made ad libitum observations of inaccuracies and misleading content. We expected that representation of age-sex classes and activity budgets in documentaries would differ from those reported in the primary literature for the same species in the wild. In addition, we expected inaccurate depictions for every species. For ring-tailed lemurs, adult males were underrepresented in documentaries. For macaques, chimpanzees, and gorillas, representation of age-sex classes did not differ significantly from observations in the wild. Documentary depictions of activity budgets differed from researcher accounts of wild primate behavior for rhesus macaques, chimpanzees, and mountain gorillas, but not for ring-tailed lemurs. In general, documentaries overrepresented traveling and social behaviors such as play and grooming. Documentaries, especially docudramas, may have emphasized traveling because such footage allows storyline narration, whereas the emphasis on social behavior was likely due to the appeal of such footage to audiences. Inaccuracies were documented for all four species, with rhesus macaques having the most inaccuracies. We propose that primatologists have an ethical imperative to enhance the accuracy of primate portrayals to audiences.

A low-cost genomics workflow enables isolate screening and strain-level analyses within microbiomes.

Earth's environments harbor complex consortia of microbes that affect processes ranging from host health to biogeochemical cycles. Understanding their evolution and function is limited by an inability to isolate genomes in a high-throughput manner. Here, we present a workflow for bacterial whole-genome sequencing using open-source labware and the OpenTrons robotics platform, reducing costs to approximately $10 per genome. We assess genomic diversity within 45 gut bacterial species from wild-living chimpanzees and bonobos. We quantify intraspecific genomic diversity and reveal divergence of homologous plasmids between hosts. This enables population genetic analyses of bacterial strains not currently possible with metagenomic data alone.

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.

Interspecific interactions between sympatric apes.

Gorillas reside in sympatry with chimpanzees over the majority of their range. Compiling all known reports of overlap between apes and augmenting these with observations made over twenty years in the Ndoki Forest, we examine the potential predation-related, foraging, and social contexts of interspecific associations between gorillas and chimpanzees. We reveal a greater diversity of interactions than previously recognized, which range from play to lethal aggression. Furthermore, there are indications that interactions between ape species may serve multiple functions. Interactions between gorillas and chimpanzees were most common during foraging activities, but they also overlapped in several other contexts. From a social perspective, we provide evidence of consistent relationships between particular chimpanzee-gorilla dyads. In addition to providing new insights into extant primate community dynamics, the diversity of interactions between apes points to an entirely new field of study in early human origins as early hominins also likely had opportunities to associate.

Zoonotic origin of the human malaria parasite Plasmodium malariae from African apes.

The human parasite Plasmodium malariae has relatives infecting African apes (Plasmodium rodhaini) and New World monkeys (Plasmodium brasilianum), but its origins remain unknown. Using a novel approach to characterise P. malariae-related sequences in wild and captive African apes, we found that this group comprises three distinct lineages, one of which represents a previously unknown, highly divergent species infecting chimpanzees, bonobos and gorillas across central Africa. A second ape-derived lineage is much more closely related to the third, human-infective lineage P. malariae, but exhibits little evidence of genetic exchange with it, and so likely represents a separate species. Moreover, the levels and nature of genetic polymorphisms in P. malariae indicate that it resulted from the zoonotic transmission of an African ape parasite, reminiscent of the origin of P. falciparum. In contrast, P. brasilianum falls within the radiation of human P. malariae, and thus reflects a recent anthroponosis.

The complex Y-chromosomal history of gorillas.

Studies of the evolutionary relationships among gorilla populations using autosomal and mitochondrial sequences suggest that male-mediated gene flow may have been important in the past, but data on the Y-chromosomal relationships among the gorilla subspecies are limited. Here, we genotyped blood and noninvasively collected fecal samples from 12 captives and 257 wild male gorillas of known origin representing all four subspecies (Gorilla gorilla gorilla, G. g. diehli, G. beringei beringei, and G. b. graueri) at 10 Y-linked microsatellite loci resulting in 102 unique Y-haplotypes for 224 individuals. We found that western lowland gorilla (G. g. gorilla) haplotypes were consistently more diverse than any other subspecies for all measures of diversity and comprised several genetically distinct groups. However, these did not correspond to geographical proximity and some closely related haplotypes were found several hundred kilometers apart. Similarly, our broad sampling of eastern gorillas revealed that mountain (G. b. beringei) and Grauer's (G. b. graueri) gorilla Y-chromosomal haplotypes did not form distinct clusters. These observations suggest structure in the ancestral population with subsequent mixing of differentiated haplotypes by male dispersal for western lowland gorillas, and postisolation migration or incomplete lineage sorting due to short divergence times for eastern gorillas.

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.

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.

Fermented food consumption in wild nonhuman primates and its ecological drivers.

OBJECTIVES: Although fermented food use is ubiquitous in humans, the ecological and evolutionary factors contributing to its emergence are unclear. Here we investigated the ecological contexts surrounding the consumption of fruits in the late stages of fermentation by wild primates to provide insight into its adaptive function. We hypothesized that climate, socioecological traits, and habitat patch size would influence the occurrence of this behavior due to effects on the environmental prevalence of late-stage fermented foods, the ability of primates to detect them, and potential nutritional benefits. MATERIALS AND METHODS: We compiled data from field studies lasting at least 9 months to describe the contexts in which primates were observed consuming fruits in the late stages of fermentation. Using generalized linear mixed-effects models, we assessed the effects of 18 predictor variables on the occurrence of fermented food use in primates. RESULTS: Late-stage fermented foods were consumed by a wide taxonomic breadth of primates. However, they generally made up 0.01%-3% of the annual diet and were limited to a subset of fruit species, many of which are reported to have mechanical and chemical defenses against herbivores when not fermented. Additionally, late-stage fermented food consumption was best predicted by climate and habitat patch size. It was more likely to occur in larger habitat patches with lower annual mean rainfall and higher annual mean maximum temperatures. DISCUSSION: We posit that primates capitalize on the natural fermentation of some fruits as part of a nutritional strategy to maximize periods of fruit exploitation and/or access a wider range of plant species. We speculate that these factors contributed to the evolutionary emergence of the human propensity for fermented foods.

The ontogeny of termite gathering among chimpanzees in the Goualougo Triangle, Republic of Congo.

OBJECTIVES: Acquiring tool-assisted foraging skills can potentially improve dietary quality and increase fitness for wild chimpanzees (Pan troglodytes). In contrast to chimpanzees in East and West Africa, chimpanzees in the Congo Basin use tool sets and brush-tipped fishing probes to gather termites. We investigated the ontogeny of these tool skills in chimpanzees of the Goualougo Triangle, Republic of Congo, and compared it to that for chimpanzees at Gombe, Tanzania. We assessed whether chimpanzees acquired simple tool behaviors and single tool use before more complex actions and sequential use of multiple tool types. MATERIALS AND METHODS: Using a longitudinal approach, we scored remote video footage to document the acquisition of termite-gathering critical elements for 25 immature chimpanzees at Goualougo. RESULTS: All chimpanzees termite fished by 2.9 years but did not manufacture brush-tipped probes until an average of 4.3 years. Acquisition of sequential tool use extended into juvenility and adolescence. While we did not detect significant sex differences, most critical elements except tool manufacture were acquired slightly earlier by females. DISCUSSION: These findings contrast with Gombe, where chimpanzees learn to both use and make fishing probes between ages 1.5-3.5 and acquire the complete task by age 5.5. Differences between sites could reflect tool material selectivity and design complexity, the challenge of sequential tool behaviors, and strength requirements of puncturing subterranean termite nests at Goualougo. These results illustrate how task complexity may influence the timing and sequence of skill acquisition, improving models of the ontogeny of tool behavior among early hominins who likely used complex, perishable technologies.