Influence of food physical properties and environmental context on manipulative behaviors highlighted by new methodological approaches in zoo-housed bonobos (Pan paniscus).

Research on manipulative abilities in nonhuman primates, in the context of hominid evolution, has mostly focused on manual/pedal postures considered as static behaviors. While these behavioral repertoires highlighted the range of manipulative abilities in many species, manipulation is a dynamic process that mostly involves successive types of grips before reaching its goal. The present study aims to investigate the use of manual/pedal postures in zoo-housed bonobos in diverse dynamic food processing by using an innovative approach: the optimal matching analysis that compares sequences (i.e., succession of grasping postures) with each other. To characterize the manipulative techniques spontaneously employed by bonobos, we performed this sequential analysis of manual/pedal postures during 766 complete feeding sequences of 17 individuals. We analyzed the effectiveness with a score defined by a partial proxy of food intake (i.e., the number of mouthfuls) linked to a handling score measuring both the diversity and changes of manual postures during each sequence. We identified four techniques, used differently depending on the physical substrate on which the individual performed food manipulation and the food physical properties. Our results showed that manipulative techniques were more complex (i.e., higher handling score) for large foods and on substrates with lower stability. But the effectiveness score was not significantly lower for these items since manipulative complexity seemed to be compensated by a greater number of mouthfuls. It appeared that the techniques employed involved a trade-off between manipulative complexity and the amount of food ingested. This study allowed us to test and validate innovative analysis methods that are applicable to diverse ethological studies involving sequential events. Our results bring new data for a better understanding of the evolution of manual abilities in primates in association with different ecological contexts and both terrestrial and arboreal substrates and suggest that social and individual influences need to be explored further.

Vertical climbing in free-ranging bonobos: An exploratory study integrating locomotor performance and substrate compliance.

OBJECTIVES: Ecological factors and body size shape animal movement and adaptation. Large primates such as bonobos excel in navigating the demanding substrates of arboreal habitats. However, current approaches lack comprehensive assessment of climbing performance in free-ranging individuals, limiting our understanding of locomotor adaptations. This study aims to explore climbing performance in free-ranging bonobos and how substrate properties affect their behavior. METHODS: We collected data on the climbing performance of habituated bonobos, Pan paniscus, in the Bolobo Territory, Democratic Republic of Congo. We analyzed 46 climbing bouts (12 ascents, 34 descents) while moving on vertical substrates of varying diameter and compliance levels. This study assessed the average speed, peak acceleration, resting postures, and transitions between climbing and other locomotor modes. RESULTS: During climbing sequences and transitions, bonobos mitigate speed variations. They also exhibit regular pauses during climbing and show higher speeds during descent in contrast to their ascent. Regarding the influence of substrate properties, bonobos exhibit higher speed when ascending on thin and slightly flexible substrates, while they appear to achieve higher speeds when descending on large and stiff substrates, by using a "fire-pole slide" submode. DISCUSSION: Bonobos demonstrate remarkable abilities for negotiating vertical substrates and substrate properties influence their performance. Our results support the idea that bonobos adopt a behavioral strategy that aligns with the notion of minimizing costs. Overall, the adoption of high velocities and the use of low-cost resting postures may reduce muscle fatigue. These aspects could represent important targets of selection to ensure ecological efficiency in bonobos.

Higher convergence of human-great ape enteric eukaryotic viromes in central African forest than in a European zoo: a One Health analysis.

Human-animal pathogenic transmissions threaten both human and animal health, and the processes catalyzing zoonotic spillover and spillback are complex. Prior field studies offer partial insight into these processes but overlook animal ecologies and human perceptions and practices facilitating human-animal contact. Conducted in Cameroon and a European zoo, this integrative study elucidates these processes, incorporating metagenomic, historical, anthropological and great ape ecological analyses, and real-time evaluation of human-great ape contact types and frequencies. We find more enteric eukaryotic virome sharing between Cameroonian humans and great apes than in the zoo, virome convergence between Cameroonian humans and gorillas, and adenovirus and enterovirus taxa as most frequently shared between Cameroonian humans and great apes. Together with physical contact from hunting, meat handling and fecal exposure, overlapping human cultivation and gorilla pillaging in forest gardens help explain these findings. Our multidisciplinary study identifies environmental co-use as a complementary mechanism for viral sharing.

Manipulative repertoire of bonobos (Pan paniscus) in spontaneous feeding situation.

Comparative behavioral studies of hand use amongst primate species, including humans, have been central in research on evolutionary mechanisms. In particular, the manipulative abilities of our closest relatives, the chimpanzee (Pan troglodytes), have been widely described in various contexts, showing a high level of dexterity both in zoo and in natural conditions. In contrast, the study of bonobos' manipulative abilities has almost exclusively been carried out in experimental contexts related to tool use. The objective of the present study is to describe the richness of the manipulative repertoire of zoo-housed bonobos, in a spontaneous feeding context including various physical substrates to gain a larger insight into our evolutionary past. Our study describes a great variety of grasping postures and grip associations in bonobos, close to the range of manipulative repertoire in chimpanzees, confirming that the two species are not markedly different in terms of cognitive and morphological constraints associated with food manipulation. We also observed differences in manipulative behaviors between juveniles and adults, indicating a greater diversity in grip associations and grasping postures used in isolation with age, and a sex-biased use of tools with females using tools more often than males. These results are consistent with the previous results in the Pan genus and reinforce the hypothesis that the evolutionary mechanisms underlying the flexibility of manipulative behaviors are shared by both species and that these ecological strategies would have already evolved in their common ancestor.

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.

A multi-disciplinary comparison of great ape gut microbiota in a central African forest and European zoo.

Comparisons of mammalian gut microbiota across different environmental conditions shed light on the diversity and composition of gut bacteriome and suggest consequences for human and animal health. Gut bacteriome comparisons across different environments diverge in their results, showing no generalizable patterns linking habitat and dietary degradation with bacterial diversity. The challenge in drawing general conclusions from such studies lies in the broad terms describing diverse habitats ("wild", "captive", "pristine"). We conducted 16S ribosomal RNA gene sequencing to characterize intestinal microbiota of free-ranging sympatric chimpanzees and gorillas in southeastern Cameroon and sympatric chimpanzees and gorillas in a European zoo. We conducted participant-observation and semi-structured interviews among people living near these great apes to understand better their feeding habits and habitats. Unexpectedly, bacterial diversity (ASV, Faith PD and Shannon) was higher among zoo gorillas than among those in the Cameroonian forest, but zoo and Cameroonian chimpanzees showed no difference. Phylogeny was a strong driver of species-specific microbial composition. Surprisingly, zoo gorilla microbiota more closely resembled that of zoo chimpanzees than of Cameroonian gorillas. Zoo living conditions and dietary similarities may explain these results. We encourage multidisciplinary approach integrating environmental sampling and anthropological evaluation to characterize better diverse environmental conditions of such investigations.

Using physical contact heterogeneity and frequency to characterize dynamics of human exposure to nonhuman primate bodily fluids in central Africa.

Emerging infectious diseases of zoonotic origin constitute a recurrent threat to global health. Nonhuman primates (NHPs) occupy an important place in zoonotic spillovers (pathogenic transmissions from animals to humans), serving as reservoirs or amplifiers of multiple neglected tropical diseases, including viral hemorrhagic fevers and arboviruses, parasites and bacteria, as well as retroviruses (simian foamy virus, PTLV) that are pathogenic in human beings. Hunting and butchering studies in Africa characterize at-risk human social groups, but overlook critical factors of contact heterogeneity and frequency, NHP species differences, and meat processing practices. In southeastern Cameroon, a region with a history of zoonotic emergence and high risk of future spillovers, we conducted a novel mixed-method field study of human physical exposure to multiple NHP species, incorporating participant-based and ecological methodologies, and qualitative interviews (n = 25). We find frequent physical contact across adult human populations, greater physical contact with monkeys than apes, especially for meat handling practices, and positive correlation of human exposure with NHP species abundance and proximity to human settlement. These fine-grained results encourage reconsideration of the likely dynamics of human-NHP contact in past and future NTD emergence events. Multidisciplinary social science and ecological approaches should be mobilized to generate more effective human and animal surveillance and risk communications around neglected tropical diseases. At a moment when the WHO has included "Disease X", a presumably zoonotic pathogen with pandemic potential, on its list of blueprint priority diseases as, new field-based tools for investigating zoonotic disease emergence, both known and unknown, are of critical importance.

Rethinking Human-Nonhuman Primate Contact and Pathogenic Disease Spillover.

Zoonotic transmissions are a major global health risk, and human-animal contact is frequently raised as an important driver of transmission. A literature examining zooanthroponosis largely agrees that more human-animal contact leads to more risk. Yet the basis of this proposition, the term contact, has not been rigorously analyzed. To understand how contact is used to explain cross-species spillovers, we conducted a multi-disciplinary review of studies addressing human-nonhuman primate (NHP) engagements and pathogenic transmissions and employing the term contact. We find that although contact is frequently invoked, it is employed inconsistently and imprecisely across these studies, overlooking the range of pathogens and their transmission routes and directions. We also examine a related but more expansive approach focusing on human and NHP habitats and their spatial overlap, which can potentially facilitate pathogenic transmission. Contact and spatial overlap investigations cannot, however, explain the processes that bring together people, animals and pathogens. We therefore examine another approach that enhances our understanding of zoonotic spillovers: anthropological studies identifying such historical, social, environmental processes. Comparable to a One Health approach, our ongoing research in Cameroon draws contact, spatial overlap and anthropological-historical approaches into dialog to suggest where, when and how pathogenic transmissions between people and NHPs may occur. In conclusion, we call for zoonotic disease researchers to specify more precisely the human-animal contacts they investigate and to attend to how broader ecologies, societies and histories shape pathogen-human-animal interactions.

How bonobo communities deal with tannin rich fruits: Re-ingestion and other feeding processes.

This report describes bonobo (Pan paniscus, Hominidae) behavioral flexibility and inter-community differences with high tannin level fruit processing. In fruiting plants, tannin should discourage certain seed dispersers (direct deterrence hypothesis) such as primates. Based on data deriving from five study sites; LuiKotale, Lomako, Wamba, Malebo and Manzano, we compare consumption and dispersal of fruit species rich in tannins: Parinari and Musanga pulp was chewed across all communities probably for saliva tannin neutralisation. However, consumption of the fruits of Canarium schweinfurthii was observed in few communities only with differences in the food process: While bonobos of Wamba, Lomako and Manzano crunched and swallowed the pulp, bonobos of LuiKotale ingested entire fruits, extracted intact fruits from feces, and re-ingested their pulp, spitting the seed after a retention time of 24h in the digestive tract (i.e. endozoochory). We discuss potential functions of this peculiar feeding technique, likely to be a cultural behavior.

Beyond the Cut Hunter: A Historical Epidemiology of HIV Beginnings in Central Africa.

In the absence of direct evidence, an imagined "cut hunter" stands in for the index patient of pandemic HIV/AIDS. During the early years of colonial rule, this explanation goes, a hunter was cut or injured from hunting or butchering a chimpanzee infected with simian immunodeficiency virus, resulting in the first sustained human infection with the virus that would emerge as HIV-1M. We argue here that the "cut hunter" relies on a historical misunderstanding and ecological oversimplification of human-chimpanzee (Pan Troglodytes troglodytes) interactions that facilitated pathogenic transmission. This initial host shift cannot explain the beginnings of the HIV/AIDS pandemic. Instead, we must understand the processes by which the virus became transmissible, possibly between Sangha basin inhabitants and ultimately reached Kinshasa. A historical epidemiology of the late nineteenth and twentieth centuries, provides a much-needed corrective to the major shortcomings of the cut hunter. Based on 62 oral historical interviews conducted in southeastern Cameroon and archival research, we show that HIV emerged from ecological, economic, and socio-political transformations of the late nineteenth and twentieth centuries. The gradual imposition of colonial rule built on and reoriented ecologies and economies, and altered older patterns of mobility and sociality. Certain changes may have contributed to the initial viral host shift, but more importantly, facilitated the adaptation of HIV-1M to human-to-human transmission. Our evidence suggests that the most critical changes occurred after 1920. This argument has important implications for public health policy, underscoring recent work emphasizing alternative pathways for zoonotic spillovers into human beings.

Intestinal Helminths of Wild Bonobos in Forest-Savanna Mosaic: Risk Assessment of Cross-Species Transmission with Local People in the Democratic Republic of the Congo.

Phylogenetic and geographic proximities between humans and apes pose a risk of zoonotic transmission of pathogens. Bonobos (Pan paniscus) of the Bolobo Territory, Democratic Republic of the Congo, live in a fragmented forest-savanna mosaic setting, a marginal habitat for this species used to living in dense forests. Human activities in the forest have increased the risk of contacts between humans and bonobos. Over 21 months (September 2010-October 2013), we monitored intestinal parasites in bonobo (n = 273) and in human (n = 79) fecal samples to acquire data on bonobo parasitology and to assess the risk of intestinal helminth transmission between these hosts. Coproscopy, DNA amplification, and sequencing of stored dried feces and larvae were performed to identify helminths. Little difference was observed in intestinal parasites of bonobos in this dryer habitat compared to those living in dense forests. Although Strongylids, Enterobius sp., and Capillaria sp. were found in both humans and bonobos, the species were different between the hosts according to egg size or molecular data. Thus, no evidence of helminth transmission between humans and bonobos was found. However, because humans and this threatened species share the same habitat, it is essential to continue to monitor this risk.

Bonobo habituation in a forest-savanna mosaic habitat: influence of ape species, habitat type, and sociocultural context.

Habituation is the term used to describe acceptance by wild animals of a human observer as a neutral element in their environment. Among primates, the process takes from a few days for Galago spp. to several years for African apes. There are also intraspecies differences reflecting differences in habitat, home range, and ape-human relationship history. Here, we present the first study of the process of bonobo habituation in a fragmented habitat, a forest-savanna mosaic in the community-based conservation area led by the Congolese nongovernmental organization Mbou-Mon-Tour, Democratic Republic of the Congo. In this area, local people use the forest almost every day for traditional activities but avoid bonobos because of a traditional taboo. Because very few flight reactions were observed during habituation, we focused on quantitative parameters to assess the development of ape tolerance and of the tracking efficiency of observer teams. During the 18-month study period (May 2012-October 2013), 4043 h (319 days) were spent in the forest and bonobos were observed for a total of 405 h (196 contacts on 134 days). The average contact duration was stable over time (124 min), but the minimal distance during a contact decreased with habituation effort. Moreover, bonobo location and tracking efficiency, daily ratio of contact time to habituation effort, and the number of observations at ground level were positively correlated with habituation effort. Our observations suggest that bonobos become habituated relatively rapidly. These results are discussed in relation to the habitat type, ape species, and the local sociocultural context of villagers. The habituation process involves changes in ape behavior toward observers and also more complex interactions concerning the ecosystem, including the building of an efficient local team. Before starting a habituation process, knowledge of the human sociocultural context is essential to assess the balance between risks and benefits.

Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: role of sociality and physiology on learning process.

Certain toxic plants are beneficial for health if small amounts are ingested infrequently and in a specific context of illness. Among our closest living relatives, chimpanzees are found to consume plants with pharmacological properties. Providing insight on the origins of human self-medication, this study investigates the role social systems and physiology (namely gut specialization) play on learning mechanisms involved in the consumption of unusual and potentially bioactive foods by two great ape species. We collected data from a community of 41-44 wild chimpanzees in Uganda (11 months, 2008), and a group of 11-13 wild western gorillas in Central African Republic (10 months, 2008-2009). During feeding, we recorded food consumed, its availability, and social interactions (including observers watching conspecifics and the observers' subsequent activity). Unusual food consumption in chimpanzees was twice higher than in gorillas. Additionally chimpanzees relied more on social information with vertical knowledge transmission on unusual foods by continually acquiring information during their life through mostly observing the fittest (pre-senescent) adults. In contrast, in gorillas observational learning primarily occurred between related immatures, showing instead the importance of horizontal knowledge transmission. As chimpanzees' guts are physiologically less specialized than gorillas (more capable of detoxifying harmful compounds), unusual-food consumption may be more risky for chimpanzees and linked to reasons other than nutrition (like self-medication). Our results show that differences in sociality and physiology between the two species may influence mechanisms that discriminate between plants for nutrition and plants with potential therapeutic dietary components. We conclude that self-medication may have appeared in our ancestors in association with high social tolerance and lack of herbivorous gut specialization.

[Nematodes of the genus Oesophagostomum: an emerging risk for humans and apes in Africa?]. / Les nématodes du genre Oesophagostomum. Un risque émergent pour l'homme et les grands singes en Afrique?

Nematodes of the genus Oesophagostomum are common intestinal parasites found in cattle, pigs and primates. They can cause severe illness, resulting from the formation of granulomas, caseous lesions and abscesses in the intestinal wall. Human oesophagostomosis is endemic in northern Ghana and Togo. In these regions, epidemiological investigations have been conducted to determine the biological characteristics, transmission dynamics and optimal management of clinical cases. Nodular oesophagostomosis has also been described in free-ranging chimpanzees and gorillas. Clinical signs associated with nodules have been observed in great apes raised in sanctuaries, while the health status of their wild counterparts does not seem to be significantly affected It has been suggested that some nonhuman primates may act as reservoirs for human oesophagostomosis. In Ghana, identification of genetic differences among Oesophagostomum nematodes infecting different primate hosts suggests that oesophagostomosis is a rare zoonosis. In Uganda, where the situation is diferent, cross-infection is probably more frequent.