Wild Apes Research Articles

Habituating field scientists.

This article explores the sensory dimensions of scientific field research in the only region in the world where free-ranging bonobos ( Pan paniscus) can be studied in their natural environment; the equatorial rainforest of the Democratic Republic of Congo. If, as sensory anthropologists have argued, the senses are developed, grown and honed in a given cultural and environmental milieu, how is it that field scientists come to dwell among familiarity in a world which is, at first, unfamiliar? This article builds upon previous anthropological and philosophical engagements with habituation that have critically examined primatologists' attempts to become 'neutral objects in the environment' in order to habituate wild apes to their presence. It does so by tracing the somatic modes of attention developed by European and North American researchers as they follow bonobos in these forests. The argument is that as environments, beings and their elements become familiar, they do not become 'neutral', but rather, suffused with meaning.

Hair plucking, stress, and urinary cortisol among captive bonobos (Pan paniscus).

Hair plucking has been observed in many captive primate species, including the great apes; however, the etiology of this behavioral pattern is poorly understood. While this behavior has not been reported in wild apes, an ethologically identical behavior in humans, known as trichotillomania, is linked to chronic psychosocial stress and is a predominantly female disorder. This study examines hair plucking (defined here as a rapid jerking away of the hair shaft and follicle by the hand or mouth, often accompanied by inspection and consumption of the hair shaft and follicle) in a captive group of bonobos (N = 13) at the Columbus Zoo and Aquarium in Columbus, Ohio. Plucking data were collected using behavior and all-occurrence sampling; 1,450 social and self-directed grooming bouts were recorded during 128 hr of observation. Twenty-one percent of all grooming bouts involved at least one instance of plucking. Urine samples (N = 55) were collected and analyzed for the stress hormone cortisol. Analyses of urinary cortisol levels showed a significant positive correlation between mean cortisol and self-directed plucking for females (r = 0.88, P < 0.05) but not for males (r = -0.73, P = 0.09). These results demonstrate an association between relative self-directed hair plucking and cortisol among female bonobos. This is the first study to investigate the relationship between hair plucking and cortisol among apes. Overall, these data add to our knowledge of a contemporary issue in captive ape management. Zoo Biol. 35:415-422, 2016. © Wiley Periodicals, Inc.

Epidemiological Surveillance of Lymphocryptovirus Infection in Wild Bonobos

Lymphocryptovirus (LCV) is one of the major gena in the herpesvirus family and is widely disseminated among primates. LCVs of human and rhesus macaques are shown to be causative agents of a number of malignant diseases including lymphoma and carcinoma. Bonobos (Pan paniscus) are highly endangered and the least studied species of the great apes. Considering the potential pathogenicity of the LCV that might threaten the fate of wild bonobos, population-based epidemiological information in terms of LCV prevalence in different location of Bonobo’s habitats will help propose improved conservation strategies for the bonobos. However, such data are not available yet because it is very difficult to collect blood samples in the wild and thus virtually impossible to conduct sero-epidemiological study on the wild ape. In order to overcome this issue, we focused on evaluating anti-LCV IgA in the feces of bonobos, which are available in a non-invasive manner. Preliminary study showed that anti-LCV IgA but not IgG was efficiently and reproducibly detected in the feces of captive chimpanzees. It is noteworthy that the fecal IgA-positive individuals were seropositive for both anti-LCV IgG and IgA and that the IgA antibodies in both sera and feces were also detectable by Western blotting assay. These results indicate that the detection of fecal anti-LCV IgA is likely a reliable and feasible for epidemiological surveillance of LCV prevalence in the great apes. We then applied this method and found that 31% of wild bonobos tested were positive for anti-LCV IgA antibody in the feces. Notably, the positivity rates varied extensively among their sampled populations. In conclusion, our results in this study demonstrate that LCV is highly disseminated among wild bonobos while the prevalence is remarkably diverse in their population-dependent manner.

Codetection of Respiratory Syncytial Virus in Habituated Wild Western Lowland Gorillas and Humans During a Respiratory Disease Outbreak.

Pneumoviruses have been identified as causative agents in several respiratory disease outbreaks in habituated wild great apes. Based on phylogenetic evidence, transmission from humans is likely. However, the pathogens have never been detected in the local human population prior to or at the same time as an outbreak. Here, we report the first simultaneous detection of a human respiratory syncytial virus (HRSV) infection in western lowland gorillas (Gorilla gorilla gorilla) and in the local human population at a field program in the Central African Republic. A total of 15 gorilla and 15 human fecal samples and 80 human throat swabs were tested for HRSV, human metapneumovirus, and other respiratory viruses. We were able to obtain identical sequences for HRSV A from four gorillas and four humans. In contrast, we did not detect HRSV or any other classic human respiratory virus in gorilla fecal samples in two other outbreaks in the same field program. Enterovirus sequences were detected but the implication of these viruses in the etiology of these outbreaks remains speculative. Our findings of HRSV in wild but human-habituated gorillas underline, once again, the risk of interspecies transmission from humans to endangered great apes.

Lateralization and performance asymmetries in the termite fishing of wild chimpanzees in the goualougo triangle, republic of Congo.

The nearly universal right hand preference manifested by human populations is one of the most pronounced manifestations of population-level lateralization. Morphological and archeological evidence indicate that this behavioral specialization may have emerged among our hominin ancestors. Whether population-level behavioral asymmetries are evident in non-human animals remains a topic of considerable scientific debate, with the most consistent evidence of population-level trends emerging from studies of chimpanzees (Pan troglodytes). However, previous studies of population-level lateralization in wild apes have relied upon data sets pooled across populations to reach adequate sample sizes. Our aim was to test for population-level handedness within a single wild chimpanzee population, and also to determine if performance asymmetries were associated with handedness. To address these questions, we coded handedness and duration of fishing probe insertions from remote video footage of chimpanzee visitation to termite nests (totaling 119 hr) in the Goualougo Triangle, Republic of Congo. Similar to reports from other populations, chimpanzees in the Goualougo Triangle showed robust individual hand preferences for termite fishing. There were 46 right-handed, 39 left-handed, and 4 ambiguously-handed individuals. Though we did not detect an overall significant population-level handedness (t(88) = 0.83, n.s.) in this study, males showed a greater right hand preference than females. Further, we found that average dipping latencies were significantly faster for right- compared to left-handed chimpanzees. Possible explanations and evolutionary implications of taxa- and task-specific patterns of population-level laterality are discussed. Am. J. Primatol. 78:1190-1200, 2016. © 2016 Wiley Periodicals, Inc.

Socioecological correlates of clinical signs in two communities of wild chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania.

Disease and other health hazards pose serious threats to the persistence of wild ape populations. The total chimpanzee population at Gombe National Park, Tanzania, has declined from an estimated 120 to 150 individuals in the 1960's to around 100 individuals by the end of 2013, with death associated with observable signs of disease as the leading cause of mortality. In 2004, we began a non-invasive health-monitoring program in the two habituated communities in the park (Kasekela and Mitumba) with the aim of understanding the prevalence of health issues in the population, and identifying the presence and impacts of various pathogens. Here we present prospectively collected data on clinical signs (observable changes in health) in the chimpanzees of the Kasekela (n = 81) and Mitumba (n = 32) communities over an 8-year period (2005-2012). First, we take a population approach and analyze prevalence of clinical signs in five different categories: gastrointestinal system (diarrhea), body condition (estimated weight loss), respiratory system (coughing, sneezing etc.), wounds/lameness, and dermatologic issues by year, month, and community membership. Mean monthly prevalence of each clinical sign per community varied, but typically affected <10% of observed individuals. Secondly, we analyze the presence of clinical signs in these categories as they relate to individual demographic and social factors (age, sex, and dominance rank) and simian immunodeficiency virus (SIVcpz) infection status. Adults have higher odds of being observed with diarrhea, loss of body condition, and wounds or lameness when compared to immatures, while males have a higher probability of being observed with wounds or lameness than females. In contrast, signs of respiratory illness appear not to be related to chimpanzee-specific factors and skin abnormalities are very rare. For a subset of known-rank individuals, dominance rank predicts the probability of wounding/lameness in adult males, but does not predict any adverse clinical signs in adult females. Instead, adult females with SIVcpz infection are more likely to be observed with diarrhea, a finding that warrants further investigation. Comparable data are needed from other sites to determine whether the prevalence of clinical signs we observe are relatively high or low, as well as to more fully understand the factors influencing health of wild apes at both the population and individual level. Am. J. Primatol. 80:e22562, 2018. © 2016 Wiley Periodicals, Inc.

Non-invasive quantification of immunoglobulin A in chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania.

Immunoglobulin A (IgA) is the primary antibody responsible for mucosal defense in mammals and has been used as a marker for chronic stress and immune status. Therefore, this antibody may provide a more reliable indicator of an individual's immunocompetence than is currently available through other methods. Immunoglobulin A has never before been quantified in a wild population of non-human primates using non-invasive sample collection techniques. In this study, we present methodology for non-invasive IgA extraction in the field and provide quantification of mean fecal IgA concentrations in wild chimpanzees (Pan troglodytes schweinfurthii). During the study period (November 2009-October 2010), we collected fecal samples (N = 1463) from 59 individuals at Gombe National Park, Tanzania. We modified a field extraction technique for steroidal hormones to extract IgA from the fecal samples and then quantified mean IgA concentrations (ng/g) using a commercial human IgA enzyme immunoassay. Mean IgA concentration varied among individuals but not by sex or reproductive status. Mature animals tended toward higher mean IgA concentration than immature. Mean IgA concentration differed by quartile season, following a similar pattern previously observed for respiratory illness rates in this population, with the late dry season having significantly higher averages than the late wet. A circadian rhythm was also evident with mean IgA concentrations higher in samples collected in the latter half of the day. These demographic and temporal patterns of IgA concentration provide baseline values necessary to interpret future results, which may be combined with other health values to better understand the role of health and long-term stress in wild great ape populations. Am. J. Primatol. 80:e22558, 2018. © 2016 Wiley Periodicals, Inc.

Ape malaria transmission and potential for ape-to-human transfers in Africa

Recent studies have highlighted the large diversity of malaria parasites infecting African great apes (subgenus Laverania) and their strong host specificity. Although the existence of genetic incompatibilities preventing the cross-species transfer may explain host specificity, the existence of vectors with a high preference for a determined host represents another possibility. To test this hypothesis, we undertook a 15-mo-long longitudinal entomological survey in two forest regions of Gabon, where wild apes live, at different heights under the canopy. More than 2,400 anopheline mosquitoes belonging to 18 species were collected. Among them, only three species of Anopheles were found infected with ape Plasmodium: Anopheles vinckei, Anopheles moucheti, and Anopheles marshallii Their role in transmission was confirmed by the detection of the parasites in their salivary glands. Among these species, An. vinckei showed significantly the highest prevalence of infection and was shown to be able to transmit parasites of both chimpanzees and gorillas. Transmission was also shown to be conditioned by seasonal factors and by the heights of capture under the canopy. Moreover, human landing catches of sylvan Anopheles demonstrated the propensity of these three vector species to feed on humans when available. Our results suggest therefore that the strong host specificity observed in the Laveranias is not linked to a specific association between the vertebrate host and the vector species and highlight the potential role of these vectors as bridge between apes and humans.

Young children spontaneously invent wild great apes' tool-use behaviours.

The variety and complexity of human-made tools are unique in the animal kingdom. Research investigating why human tool use is special has focused on the role of social learning: while non-human great apes acquire tool-use behaviours mostly by individual (re-)inventions, modern humans use imitation and teaching to accumulate innovations over time. However, little is known about tool-use behaviours that humans can invent individually, i.e. without cultural knowledge. We presented 2- to 3.5-year-old children with 12 problem-solving tasks based on tool-use behaviours shown by great apes. Spontaneous tool use was observed in 11 tasks. Additionally, tasks which occurred more frequently in wild great apes were also solved more frequently by human children. Our results demonstrate great similarity in the spontaneous tool-use abilities of human children and great apes, indicating that the physical cognition underlying tool use shows large overlaps across the great ape species. This suggests that humans are neither born with special physical cognition skills, nor that these skills have degraded due to our species’ long reliance of social learning in the tool-use domain.

Androgen receptor and monoamine oxidase polymorphism in wild bonobos

Androgen receptor gene (AR), monoamine oxidase A gene (MAOA) and monoamine oxidase B gene (MAOB) have been found to have associations with behavioral traits, such as aggressiveness, and disorders in humans. However, the extent to which similar genetic effects might influence the behavior of wild apes is unclear. We examined the loci AR glutamine repeat (ARQ), AR glycine repeat (ARG), MAOA intron 2 dinucleotide repeat (MAin2) and MAOB intron 2 dinucleotide repeat (MBin2) in 32 wild bonobos, Pan paniscus, and compared them with those of chimpanzees, Pan troglodytes, and humans. We found that bonobos were polymorphic on the four loci examined. Both loci MAin2 and MBin2 in bonobos showed a higher diversity than in chimpanzees. Because monoamine oxidase influences aggressiveness, the differences between the polymorphisms of MAin2 and MBin2 in bonobos and chimpanzees may be associated with the differences in aggression between the two species. In order to understand the evolution of these loci and AR, MAOA and MAOB in humans and non-human primates, it would be useful to conduct future studies focusing on the potential association between aggressiveness, and other personality traits, and polymorphisms documented in bonobos.

Comparative Pathology of Aging Great Apes

The great apes (chimpanzees, bonobos, gorillas, and orangutans) are our closest relatives. Despite the many similarities, there are significant differences in aging among apes, including the human ape. Common to all are dental attrition, periodontitis, tooth loss, osteopenia, and arthritis, although gout is uniquely human and spondyloarthropathy is more prevalent in apes than humans. Humans are more prone to frailty, sarcopenia, osteoporosis, longevity past reproductive senescence, loss of brain volume, and Alzheimer dementia. Cerebral vascular disease occurs in both humans and apes. Cardiovascular disease mortality increases in aging humans and apes, but coronary atherosclerosis is the most significant type in humans. In captive apes, idiopathic myocardial fibrosis and cardiomyopathy predominate, with arteriosclerosis of intramural coronary arteries. Similar cardiac lesions are occasionally seen in wild apes. Vascular changes in heart and kidneys and aortic dissections in gorillas and bonobos suggest that hypertension may be involved in pathogenesis. Chronic kidney disease is common in elderly humans and some aging apes and is linked with cardiovascular disease in orangutans. Neoplasms common to aging humans and apes include uterine leiomyomas in chimpanzees, but other tumors of elderly humans, such as breast, prostate, lung, and colorectal cancers, are uncommon in apes. Among the apes, chimpanzees have been best studied in laboratory settings, and more comparative research is needed into the pathology of geriatric zoo-housed and wild apes. Increasing longevity of humans and apes makes understanding aging processes and diseases imperative for optimizing quality of life in all the ape species.

Early Alzheimer's disease–type pathology in the frontal cortex of wild mountain gorillas (Gorilla beringei beringei)

Amyloid beta (Aβ) and tau pathology have been described in the brains of captive aged great apes, but the natural progression of these age-related pathologies from wild great apes, including the gorilla, is unknown. In our previous study of Western lowland gorillas (Gorilla gorilla gorilla) who were housed in American Zoos and Aquariums–accredited facilities, we found an age-related increase in Aβ-positive plaques and vasculature, tau-positive astrocytes, oligodendrocyte coiled bodies, and neuritic clusters in the neocortex as well as hippocampus in older animals. Here, we demonstrate that aged wild mountain gorillas (Gorilla beringei beringei), who spent their entire lives in their natural habitat, also display an age-related increase in amyloid precursor protein (APP) and/or Aβ-immunoreactive blood vessels and plaques, but very limited tau pathology, in the frontal cortex. These results indicate that Aβ and tau lesions are age-related events that occur in the brain of gorillas living in captivity and in the wild.

How similar are nut-cracking and stone-flaking? A functional approach to percussive technology.

Various authors have suggested similarities between tool use in early hominins and chimpanzees. This has been particularly evident in studies of nut-cracking which is considered to be the most complex skill exhibited by wild apes, and has also been interpreted as a precursor of more complex stone-flaking abilities. It has been argued that there is no major qualitative difference between what the chimpanzee does when he cracks a nut and what early hominins did when they detached a flake from a core. In this paper, similarities and differences between skills involved in stone-flaking and nut-cracking are explored through an experimental protocol with human subjects performing both tasks. We suggest that a 'functional' approach to percussive action, based on the distinction between functional parameters that characterize each task and parameters that characterize the agent's actions and movements, is a fruitful method for understanding those constraints which need to be mastered to perform each task successfully, and subsequently, the nature of skill involved in both tasks.

Two Cases of Cleft Lip and Other Congenital Anomalies in Wild Chimpanzees Living in Kibale National Park, Uganda.

Observations of wild chimpanzees ( Pan troglodytes schweinfurthii) were conducted in Kibale National Park, Uganda, at the sites of Sebitoli and Ngogo. We report the first two cases of cleft lip in wild chimpanzees. Additionally, some other chimpanzees in the Sebitoli community show facial dysplasia and congenital anomalies, such as patches of depigmented hairs and limb defects. Cleft lip has been documented in several species of nonhuman primates, but much remains unknown about the occurrence of cleft lip and cleft palate in great apes, probably because such malformations are rare, wild apes are difficult to monitor and observe, and severe cases associated with cleft palates render suckling impossible and lead to early death of infants. The genetic basis of such defects in great apes warrants investigation, as does the possibility that environmental toxins contribute to their etiology in Kibale in ways that could affect humans as well.

One Health, Vaccines and Ebola: The Opportunities for Shared Benefits.

The 2013 Ebola virus outbreak in West Africa, as of writing, is declining in reported human cases and mortalities. The resulting devastation caused highlights how health systems, in particular in West Africa, and in terms of global pandemic planning, are ill prepared to react to zoonotic pathogens. In this paper we propose One Health as a strategy to prevent zoonotic outbreaks as a shared goal: that human and Great Ape vaccine trials could benefit both species. Only recently have two phase 2/3 Ebola human vaccine trials been started in West Africa. This paper argues for a conceptual change in pandemic preparedness. We first discuss the ethics of One Health. Next, we focus on the current Ebola outbreak and defines its victims. Third, we present the notion of a ‘shared benefit’ approach, grounded in One Health, and argue for the vaccination of wild apes in order to protect both apes and humans. We believe that a creation of such inter-species immunity is an exemplar of One Health, and that it is worth pursuing as a coextensive public health approach.

Pointing and pantomime in wild apes? Female bonobos use referential and iconic gestures to request genito-genital rubbing.

Referential and iconic gesturing provide a means to flexibly and intentionally share information about specific entities, locations, or goals. The extent to which nonhuman primates use such gestures is therefore of special interest for understanding the evolution of human language. Here, we describe novel observations of wild female bonobos (Pan paniscus) using referential and potentially iconic gestures to initiate genito-genital (GG) rubbing, which serves important functions in reducing social tension and facilitating cooperation. We collected data from a habituated community of bonobos at Luikotale, DRC, and analysed n = 138 independent gesture bouts made by n = 11 females. Gestures were coded in real time or from video. In addition to meeting the criteria for intentionality, in form and function these gestures resemble pointing and pantomime–two hallmarks of human communication–in the ways in which they indicated the relevant body part or action involved in the goal of GG rubbing. Moreover, the gestures led to GG rubbing in 83.3% of gesture bouts, which in turn increased tolerance in feeding contexts between the participants. We discuss how biologically relevant contexts in which individuals are motivated to cooperate may facilitate the emergence of language precursors to enhance communication in wild apes.

Phylogenomic evidence for recombination of adenoviruses in wild gorillas.

Human adenoviruses (HAdVs) of species Human mastadenovirus B (HAdV-B) are genetically highly diverse and comprise several pathogenic types. AdVs closely related to members of HAdV-B infect African great apes and the evolutionary origin of HAdV-B has recently been determined in ancient gorillas. Genetic evidence for intra- and inter-species recombination has been obtained for AdVs of humans and captive great apes, but evidence from wild great apes is lacking. In this study, potential HAdV-B members of wild Eastern gorillas were analysed for evidence of recombination. One near-complete genome was amplified from primary sample material and sequenced, and from another six individuals genome fragments were obtained. In phylogenomic analysis, their penton base, pVII-pVI, hexon and fiber genes were compared with those of all publicly available HAdV-B full-genome sequences of humans and captive great apes. Evidence for intra-species recombination between different HAdV-B members of wild gorillas as well as between HAdV-B members of chimpanzees and gorillas was obtained. Since zoonotic AdVs have been reported to cause respiratory outbreaks in both humans and monkeys, and humans in West and Central Africa frequently hunt and butcher primates thereby increasing the chance of zoonotic transmission, such HAdV-B recombinants might widen the pool of potential human pathogens.

Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: Evidence of Trichomonadidae infections.

Sexually transmitted diseases (STDs) can persist endemically, are known to cause sterility and infant mortality in humans, and could have similar impacts in wildlife populations. African apes (i.e., chimpanzees, bonobos, and to a lesser extent gorillas) show multi-male mating behavior that could offer opportunities for STD transmission, yet little is known about the prevalence and impact of STDs in this endangered primate group. We used serology and PCR-based detection methods to screen biological samples from wild and orphaned eastern chimpanzees and gorillas (N = 172 individuals, including adults, and juveniles) for four classes of pathogens that either commonly cause human STDs or were previously detected in captive apes: trichomonads, Chlamydia spp., Treponema pallidum (syphilis and yaws), and papillomaviruses. Based on results from prior modeling and comparative research, we expected STD prevalence to be highest in females versus males and in sexually mature versus immature individuals. All samples were negative for Chlamydia, Treponema pallidum, and papillomaviruses; however, a high percentage of wild chimpanzee urine and fecal samples showed evidence of trichomonads (protozoa). Analysis revealed that females were more likely than males to have positive urine-but not fecal-samples; however, there was no evidence of age (sexual maturity) differences in infection status. Sequence analysis of chimpanzee trichomonad samples revealed a close relationship to previously described trichomonads within the genus Tetratrichomonas. Phylogenetic comparisons to archived sequences from multiple vertebrate hosts suggests that many of the chimpanzee parasites from our study are likely transmitted via fecal-oral contact, but the transmission of some Tetratrichomonas sequence-types remains unknown and could include sexual contact. Our work emphasizes that only a fraction of infectious agents affecting wild apes are presently known to science, and that further work on great ape STDs could offer insights for the management of endangered great apes and for understanding human STD origins.

A cautionary note on fecal sampling and molecular epidemiology in predatory wild great apes.

Fecal samples are an important source of information on parasites (viruses, prokaryotes, or eukaryotes) infecting wild great apes. Molecular analysis of fecal samples has already been used for deciphering the origins of major human pathogens such as HIV-1 or Plasmodium falciparum. However, for apes that hunt (chimpanzees and bonobos), detection of parasite nucleic acids may reflect either true infection of the host of interest or ingestion of an infected prey, for example, another non-human primate. To determine the potential magnitude of this issue, we estimated the prevalence of prey DNA in fecal samples obtained from two wild chimpanzee communities. We observed values >15%, which are higher than or close to the fecal detection rates of many great ape parasites. Contamination of fecal samples with parasite DNA from dietary origin may therefore occasionally impact non-invasive epidemiological studies. This problem can be addressed (at least partially) by monitoring the presence of prey DNA.

Tools to tipple: ethanol ingestion by wild chimpanzees using leaf-sponges.

African apes and humans share a genetic mutation that enables them to effectively metabolize ethanol. However, voluntary ethanol consumption in this evolutionary radiation is documented only in modern humans. Here, we report evidence of the long-term and recurrent ingestion of ethanol from the raffia palm (Raphia hookeri, Arecaceae) by wild chimpanzees (Pan troglodytes verus) at Bossou in Guinea, West Africa, from 1995 to 2012. Chimpanzees at Bossou ingest this alcoholic beverage, often in large quantities, despite an average presence of ethanol of 3.1% alcohol by volume (ABV) and up to 6.9% ABV. Local people tap raffia palms and the sap collects in plastic containers, and chimpanzees use elementary technology—a leafy tool—to obtain this fermenting sap. These data show that ethanol does not act as a deterrent to feeding in this community of wild apes, supporting the idea that the last common ancestor of living African apes and modern humans was not averse to ingesting foods containing ethanol.