Applying collocation and APRIORI analyses to chimpanzee diets: Methods for investigating nonrandom food combinations in primate self-medication.

Identifying novel medicinal resources in chimpanzee diets has historically presented challenges, requiring extensive behavioral data collection and health monitoring, accompanied by expensive pharmacological analyses. When putative therapeutic self-medicative behaviors are observed, these events are often considered isolated occurrences, with little attention paid to other resources ingested in combination. For chimpanzees, medicinal resource combinations could play an important role in maintaining well-being by tackling different symptoms of an illness, chemically strengthening efficacy of a treatment, or providing prophylactic compounds that prevent future ailments. We call this concept the self-medicative resource combination hypothesis. However, a dearth of methodological approaches for holistically investigating primate feeding ecology has limited our ability to identify nonrandom resource combinations and explore potential synergistic relationships between medicinal resource candidates. Here we present two analytical tools that test such a hypothesis and demonstrate these approaches on feeding data from the Sonso chimpanzee community in Budongo Forest, Uganda. Using 4 months of data, we establish that both collocation and APRIORI analyses are effective exploratory tools for identifying binary combinations, and that APRIORI is effective for multi-item rule associations. We then compare outputs from both methods, finding up to 60% agreement, and propose APRIORI as more effective for studies requiring control over confidence intervals and those investigating nonrandom associations between more than two resources. These analytical tools, which can be extrapolated across the animal kingdom, can provide a cost-effective and efficient method for targeting resources for further pharmacological investigation, potentially aiding in the discovery of novel medicines.

Chimpanzees communicate to coordinate a cultural practice.

Human culture thrives by virtue of communication, yet whether communication plays an influential role in the cultural lives of other animals remains understudied. Here, we investigated whether chimpanzees use communication to engage in a cultural practice by analysing grooming handclasp (GHC) interactions-a socio-cultural behaviour requiring interindividual coordination for successful execution. Previous accounts attributed GHC initiations to behavioural shaping, whereby the initiator physically moulds the partner's arm into the desired GHC posture. Using frame-by-frame analysis and matched-control methodology, we find that chimpanzees do not only shape their partner's posture (22%), but also use gestural communication to initiate GHC (44%), which requires an active and synchronized response from the partner. Moreover, in a third (34%) of the GHC initiations, the requisite coordination was achieved by seemingly effortless synchrony. Lastly, using a longitudinal approach, we find that for GHC initiations, communication occurs more frequently than shaping in experienced dyads and less in mother-offspring dyads. These findings are consistent with ontogenetic ritualization, thereby reflecting first documentation of chimpanzees communicating to coordinate a cultural practice. We conclude that chimpanzees show interactional flexibility in the socio-cultural domain, opening the possibility that the interplay between communication and culture is rooted in our deep evolutionary history.

Successful surgical correction of a cataract in a chimpanzee (Pan troglodytes) via field setting at a zoological facility.

A 41-year-old male vasectomized, zoo-housed chimpanzee (Pan troglodytes) presented with progressive visual deficits due to bilateral cataract formation. Phacoemulsification and lenticular implant were performed by a veterinary and human board-certified ophthalmologist team in a field setting. Post-operative healing occurred without complication, and the patient returned to the troop with improved vision.

Male-male relationships in chimpanzees and the evolution of human pair bonds.

The evolution of monogamy has been a central question in biological anthropology. An important avenue of research has been comparisons across "socially monogamous" mammals, but such comparisons are inappropriate for understanding human behavior because humans are not "pair living" and are only sometimes "monogamous." It is the "pair bond" between reproductive partners that is characteristic of humans and has been considered unique to our lineage. I argue that pair bonds have been overlooked in one of our closest living relatives, chimpanzees. These pair bonds are not between mates but between male "friends" who exhibit enduring and emotional social bonds. The presence of such bonds in male-male chimpanzees raises the possibility that pair bonds emerged earlier in our evolutionary history. I suggest pair bonds first arose as "friendships" and only later, in the human lineage, were present between mates. The mechanisms for these bonds were co-opted for male-female bonds in humans.

Simia langobardorum: Were African apes traded in late medieval Lombardy?

Depictions of and references to apes (tailless hominoids) are very limited in early historical written accounts. The first known published representations of ape-like primates appear in Medieval European books during the first century following the invention of printing. Considering the current knowledge of ape iconography, this article examines an unusual image of a couple of ape-like creatures rendered in a European manuscript and explores the possible links of this challenging illustration with historical accounts and contexts during the late Middle Ages and early Renaissance. The studied manuscript is known as "BL Sloane MS 4016" and is a medieval herbal manuscript (Tratactus de Herbis) of Lombardian origin dated c. 1440. The illustration in question, which also appears in similar manuscripts, represents two primates. However, these representations differ significantly from those in the other manuscripts. The individuals have physical features that suggest attribution to chimpanzees. The location and the date of the manuscript in relation to the extended merchant and travel network between Europe and Africa during the late Medieval times and earlier Renaissance most likely indicate that free-living or traded chimpanzees or their images may have been the visual source for the illustration. The examination of early depictions and descriptions of apes helps us to understand how we, humans, have represented our own closest zoological relatives. In doing so, this study also provides a review of early ape iconography and historical accounts about African primates during the so-called Age of Discoveries.

An intentional cohesion call in male chimpanzees of Budongo Forest.

Many social animals travel in cohesive groups but some species, including chimpanzees, form flexible fission-fusion systems where individuals have some control over group cohesion and proximity to others. Here, we explored how male chimpanzees of the Sonso community of Budongo Forest, Uganda, use communication signals during resting, a context where the likelihood of group fission is high due to forthcoming travel. We focused on a context-specific vocalisation, the 'rest hoo', to investigate its function and determine whether it is produced intentionally. We found that this call was typically given towards the end of typical silent resting bouts, i.e., the period when individuals need to decide whether to continue travelling after a brief stop-over or to start a prolonged resting bout. Subjects rested longer after producing 'rest hoos' and their resting time increased with the number of calls produced. They also rested longer if their calls were answered. Furthermore, focal subjects' resting time was prolonged after hearing others' 'rest hoos'. Subjects called more when with top proximity partners and in small parties and rested longer if a top proximity partner called. We also found an interaction effect between rank and grooming activity, with high-ranking males with a high grooming index calling less frequently than other males, suggesting that vocal communication may serve as a cohesion strategy alternative to tactile-based bonding. We discuss these different patterns and conclude that chimpanzee 'rest hoos' meet key criteria for intentional signalling. We suggest that 'rest hoos' are produced to prolong resting bouts with desired partners, which may function to increase social cohesion.

Repellent activity against Anopheles gambiae of the leaves of nesting trees in the Sebitoli chimpanzee community of Kibale National Park, Uganda.

BACKGROUND: Every evening, chimpanzees (Pan troglodytes) build a sleeping platform so called "nest" by intertwining branches of tree. Most of chimpanzees' communities studied have a preference for tree species in which they nest. As female mosquitoes are feeding on the blood of their host at nighttime, chimpanzees may prevent being disturbed and bitten by mosquitoes by selecting tree species having properties to repel them. METHODS: To test the hypothesis that chimpanzees choose tree species for their aromatic properties, data related to 1,081 nesting trees built between 2017 and 2019 in the Sebitoli community of Kibale National Park (Uganda) were analysed. The 10 most used trees were compared to the 10 most common trees in the habitat that were not preferred for nesting. Leaves from the 20 trees species were collected and hydro-distillated to obtain essential oils and one of the by-products for behavioural bioassays against females of the African mosquito, Anopheles gambiae. RESULTS: Sebitoli chimpanzees showed tree preferences: 10 species correspond to more than 80% of the nesting trees. Out of the essential oil obtained from the 10 nesting trees, 7 extracts for at least one concentration tested showed spatial repellency, 7 were irritant by contact and none were toxic. In the other hand, for the abundant trees in their habitat not used by chimpanzees, only 3 were repellent and 5 irritants. DISCUSSION AND CONCLUSION: This study contributes to evidence that chimpanzees, to avoid annoying mosquitoes, may select their nesting trees according to their repellent properties (linked to chemical parameters), a potential inspiration for human health.

The effect of warning signs on the presence of snare traps in a Ugandan rainforest.

Since chimpanzee (Pan troglodytes) conservation often involves local human populations, conservation strategies must consider psychological factors that impact their behavior. In Budongo Forest, Uganda, for example, local communities commonly engage in snare trap (hereafter: snare) setting for wild meat. This illegal activity posits a substantial threat to wild chimpanzees, causing permanent wounds or death for those who are snared. Despite various schemes previously implemented to address snare setting-an activity that is fueled by poverty, the problem and its detrimental impact on chimpanzees persists. Here, we experimentally tested a novel intervention, a systematic display of specially designed warning signs aimed at local poachers. We monitored the presence of snares before and after introducing these signs over a total period of two years and compared it with that of a similar sized control area with no intervention. Results show that snares were less likely to be present during the "sign" period than during the "non-sign" period in the experimental but not in the control area. We discuss the potential of this cost-effective intervention for limiting illegal activities that pose a severe threat to chimpanzees and other species inhabiting tropical forests.

First observation of a chimpanzee with albinism in the wild: Social interactions and subsequent infanticide.

Albinism-the congenital absence of pigmentation-is a very rare phenomenon in animals due to the significant costs to fitness of this condition. Both humans and non-human individuals with albinism face a number of challenges, such as reduced vision, increased exposure to ultraviolet radiation, or compromised crypticity resulting in an elevated vulnerability to predation. However, while observations of social interactions involving individuals with albinism have been observed in wild non-primate animals, such interactions have not been described in detail in non-human primates (hereafter, primates). Here, we report, to our knowledge, the first sighting of an infant with albinism in wild chimpanzees (Pan troglodytes schweinfurthii), including social interactions between the infant, its mother, and group members. We also describe the subsequent killing of the infant by conspecifics as well as their behavior towards the corpse following the infanticide. Finally, we discuss our observations in relation to our understanding of chimpanzee behavior or attitudes towards individuals with very conspicuous appearances.

Greetings among female chimpanzees in Mahale, Tanzania.

Greeting behaviors have been reported in several primate species, although their forms and context may vary across species. Chimpanzees (Pan troglodytes) greet each other in various ways when they meet; however, many recent studies of greetings in chimpanzees have mostly focused on pant grunt vocalizations, which are often viewed as equivalent to submissive signals. As most greetings in chimpanzees are directed toward adult males, either from other males or females, relatively few studies have focused on female-female greetings. Thus, the primary aim of this study was to describe the greetings (not limited to pant grunts) between chimpanzee females in the Mahale Mountains National Park based on long-term observational data. I observed 405 female-female greeting events (10.9 instances per 100 observation hours [obsn. h]) between 1994 and 2018, of which 242 were pant grunts (6.5 instances per 100 obsn. h); 42.3% of greetings were nonaudible, such as tactile or gestural greetings. Most pant grunts were directed toward older females; females under 20 years of age were generally responsible for this trend, as they were the most frequent greeters among females and tended to perform pant grunts toward older females. Nonetheless, among females 20 years of age or older, pant grunts from an older to a younger female were not rare (37%). Compared to previous studies in Mahale, pant grunts between females were an order of magnitude less than those directed toward males. There may also be a large difference in the frequencies of female-female pant grunts across study sites, which may be attributed to differences in female gregariousness.

Chimpanzee exposure to pollution revealed by human biomonitoring approaches.

Wildlife is increasingly exposed to environmental pollution, but data illustrating to what extent this exposure can impact health and survival of endangered species is missing. In humans, hair matrix analysis is a reliable tool for assessing cumulative exposure to organic pollutants such as pesticides but has rarely been used in other primates for this purpose. LC/MS-MS and GC/MS-MS multi-residue methods were used to screen the presence of 152 organic pollutants and their metabolites belonging to 21 different chemical families in hair samples from our closest relative, the chimpanzee. Samples were collected from 20 wild chimpanzees in Sebitoli, Kibale National Park, Uganda and 9 captive chimpanzees in the Réserve Africaine de Sigean, France. In total, 90 chemicals were detected, 60 in wild chimpanzees and 79 in captive chimpanzees. The median concentrations of detected chemicals in captive individuals were significantly higher than those in wild chimpanzees. Hair from the captive individuals at RAS was sampled a second time after 6 months in an environment of reduced exposure to these pollutants (diet of organic food, decreased use of plastic food and water containers). The number of chemicals detected in captive chimpanzees reduced from 79 to 63, and their concentrations were also significantly reduced. In the present study we report for the first time the use of hair analysis to detect organic pollutants in primate hair. We conclude that both wild and captive chimpanzees are exposed to a large range of different chemicals through their diet. Our study provides surprising and alarming evidence that besides the direct threats of poaching, deforestation and diseases, wild chimpanzees might be endangered by indirect consequences of anthropic activities. As chimpanzees are our closest relatives, our results should be considered as an alert for human health as well.

Evaluation of social compatibility in an all-male group of chimpanzees (Pan troglodytes) by means of social network analysis.

The study here presented provides preliminary data regarding social compatibility of an all-male group of five chimpanzees (Pan troglodytes), assessed by means of a social network analysis (SNA). The study was conducted at the Fundació Mona (Girona, Spain), where data on social behavior were collected in two consecutive 2-week periods using continuous focal animal sampling for a total of 72 h of observation. Our results show the study group is socially compatible: males showed high levels of affiliative behaviors (grooming) and low levels of aggressive behaviors (displacement, display, physical aggression, supplantation). In addition, these results remained stable during the two study periods. Likewise, the most central individuals in the affiliative and aggressive networks were identified, showing slight variations depending on the period of the study. Therefore, the information obtained suggests that placing male chimpanzees in all-male groups could be a potential option for the management of surplus males. The results also provide support regarding the positive contribution of social assessment to the management of captive primate groups. In this regard, SNA seems to be a useful tool to evaluate the groups' social behavior and to identify its key individuals. In addition, these results allow us to draw up a set of recommendations before the formation of an all-male group, but also to assess their compatibility once groups have been formed. As a whole, the results of this study could improve the management of endangered species like chimpanzees.

The development of affiliative and coercive reproductive tactics in male chimpanzees.

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.

Kinematic and dynamic aspects of chimpanzee knuckle walking: finger flexors likely do not buffer ground impact forces.

Chimpanzees are knuckle walkers, with forelimbs contacting the ground by the dorsum of the finger's middle phalanges. As these muscular apes are given to high-velocity motions, the question arises of how the ground reaction forces are buffered so that no damage ensues in the load-bearing fingers. In the literature, it was hypothesized that the finger flexors help buffer impacts because in knuckle stance the metacarpophalangeal joints (MCPJs) are strongly hyperextended, which would elongate the finger flexors. This stretching of the finger flexor muscle-tendon units would absorb impact energy. However, EMG studies did not report significant finger flexor activity in knuckle walking. Although these data by themselves question the finger flexor impact buffering hypothesis, the present study aimed to critically investigate the hypothesis from a biomechanical point of view. Therefore, various aspects of knuckle walking were modeled and the finger flexor tendon displacements in the load-bearing fingers were measured in a chimpanzee cadaver hand, of which also an MRI was taken in knuckle stance. The biomechanics do not support the finger flexor impact buffering hypothesis. In knuckle walking, the finger flexors are not elongated to lengths where passive strain forces would become important. Impact buffering by large flexion moments at the MCPJs from active finger flexors would result in impacts at the knuckles themselves, which is dysfunctional for various biomechanical reasons and does not occur in real knuckle walking. In conclusion, the current biomechanical analysis in accumulation of previous EMG findings suggests that finger flexors play no role in impact buffering in knuckle walking.

A machine learning approach to infant distress calls and maternal behaviour of wild chimpanzees.

Distress calls are an acoustically variable group of vocalizations ubiquitous in mammals and other animals. Their presumed function is to recruit help, but there has been much debate on whether the nature of the disturbance can be inferred from the acoustics of distress calls. We used machine learning to analyse episodes of distress calls of wild infant chimpanzees. We extracted exemplars from those distress call episodes and examined them in relation to the external event triggering them and the distance to the mother. In further steps, we tested whether the acoustic variants were associated with particular maternal responses. Our results suggest that, although infant chimpanzee distress calls are highly graded, they can convey information about discrete problems experienced by the infant and about distance to the mother, which in turn may help guide maternal parenting decisions. The extent to which mothers rely on acoustic cues alone (versus integrate other contextual-visual information) to decide upon intervening should be the focus of future research.

Systematic mapping of developmental milestones in wild chimpanzees.

Postnatal development is protracted relative to lifespan in many primates, including modern humans (Homo sapiens), facilitating the acquisition of key motor, communication and social skills that can maximize fitness later in life. Nevertheless, it remains unclear what evolutionary drivers led to extended immature periods. While the developmental milestone literature is well established in humans, insight we can gain from one-species models is limited. By comparing the timing of relatable developmental milestones in a closely related species, the chimpanzee (Pan troglodytes), we can gain further understanding of the evolution of such an extended developmental phase. To date, few studies have specifically attempted to estimate developmental milestones in a manner comparable to the human literature, and existing studies lack sufficient sample sizes to estimate which milestones are more plastic with higher inter-individual variation in the timing of their emergence. Here, we describe the emergence of gross motor, fine motor, social interaction and communication traits from a longitudinal sample of 19 wild chimpanzee infants (8 females and 11 males), Taï National Park, Côte d'Ivoire. Gross motor traits emerged at a mean of 4 months, communication traits at 12 months, social interaction traits at 14 months and fine motor traits at 15 months, with later emerging milestones demonstrating greater inter-individual variation in the timing of the emergence. This pattern of milestone emergence is broadly comparable to observations in humans, suggesting selection for a prolonged infantile phase and that sustained skills development has a deep evolutionary history, with implications for theories on primate brain development.

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.

Community-based conservation and chimpanzee research in Gishwati forest, Rwanda.

As great ape populations around the world continue to decline, largely due to anthropogenic activities, conservation programs aimed at supporting these efforts have had mixed success. Here, we evaluate our community-based conservation program in Gishwati forest, Rwanda, aimed at helping to restore biodiversity and ecosystem services using chimpanzees as a flagship species. We examine the effectiveness of this program on reducing one of the ongoing threats to Gishwati's population of chimpanzees, illegal cattle grazing as well as the program's influence on the size of the chimpanzee population. We monitored illegal cattle grazing during several study periods between 2009 and 2019 in Gishwati forest following the implementation of our conservation program in 2008 that included law enforcement, community engagement, and research components. We found that when our conservation program was active, illegal cattle grazing was reduced to low levels. We also observed an increase in the chimpanzee population size during the 11 years since we started our conservation program. We examine how this reduction in cattle grazing and increase in chimpanzee population size may have been influenced by our community-centered approach and discuss the future of our conservation work in Gishwati.

Chimpanzees (Pan troglodytes) adapt their nesting behavior after large-scale forest clearance and community decline.

Chimpanzees (Pan troglodytes) build nests at night for sleeping and occasionally during daytime for resting. Over the course of seven years, forest fragments in Bulindi, Uganda, were reduced in size by about 80% when landowners converted forest to agricultural land. However, unlike other studies on nesting behavior in response to habitat disturbance, chimpanzees at Bulindi had no opportunity to retreat into nearby undisturbed forest. To understand behavioral adaptations to forest clearance, we compared Bulindi chimpanzees' nesting characteristics before and after this period of major deforestation. After deforestation, chimpanzees built nests at lower heights in shorter trees, and reused a larger proportion of their nests. Additionally, average nest group size increased after deforestation, even though community size declined by approximately 20% over the same period. The substantial decrease in available forest habitat may have caused the chimpanzees to aggregate for nesting. However, more cohesive nesting may also have been influenced by dietary shifts (increased reliance on agricultural crops) and a need for enhanced safety with increased human encroachment. Conversely, the chimpanzees selected similar tree species for nesting after deforestation, apparently reflecting a strong preference for particular species, nested less often in exotic species, and built integrated nests (constructed using multiple trees) at a similar frequency as before fragment clearance. Chimpanzees living in unprotected habitat in Uganda, as at Bulindi, face mounting anthropogenic pressures that threaten their survival. Nevertheless, our study shows that chimpanzees can adjust their nesting behavior flexibly in response to rapid, extensive habitat change. While behavioral flexibility may enable them to cope with deforestation, at least to a certain point, the long-term survival of chimpanzees in fast-changing human-modified landscapes requires intensive conservation efforts.

Mobonda Community Conservation Project: Chimpanzees, oysters, and community engagement in Sierra Leone.

Sierra Leone constitutes the western boundary to the West Africa Upper Guinea Rainforest, one of 35 global biodiversity hotspots. The country is home to the third-largest western chimpanzee (Pan troglodytes verus) population, a subspecies upgraded to Critically Endangered on the 2016 IUCN Red List. The main threats facing chimpanzees in Sierra Leone are habitat loss and increasing interactions with humans. The Mobonda Community Conservation Project (MCCP) is a component of Tacugama Chimpanzee Sanctuary's Community Outreach Program and Kids Environmental Education Program. The aim of MCCP is to promote community-based forest management in combination with wildlife conservation through carefully designed programs that benefit communities, wildlife, and ecologically significant habitats. MCCP also aims to promote self-sustained and integrated community landscape conservation, to facilitate policy discussions to strengthen wildlife laws, and to build the capacity of the Government to implement community-based wildlife and forestry protection projects. Since Tacugama began collecting data in Moyamba District in June 2015, the project has evolved into an assembly of components. MCCP currently works with five communities, running programs including environmental education, ecological research, biomonitoring including wildlife law enforcement, habitat rehabilitation through reforestation of identified wildlife corridors, improved sustainable livelihoods, and ecotourism initiatives. These programs contributed to a reduction in the threats facing wildlife in the area; the project has seen stable chimpanzee numbers where decrements to chimpanzee populations continue to be experienced elsewhere. Other MCCP outcomes include boosted sustainable agricultural production and higher oyster yields while decreasing the negative impact on the mangrove ecosystem allowing it to recover and support an array of important fauna and flora.