Bonobos Research Articles

Hysterangium bonobo: A newly described truffle species that is eaten by bonobos in the Democratic Republic of Congo

ABSTRACT Many animals have been shown to eat fungi and most truffle-like fungi depend on animals for spore dispersal via mycophagy. Although these interactions are widespread, they are understudied in many habitats. In this study, we show that bonobos (Pan paniscus) forage and feed on an undescribed truffle species in the rainforests of the Democratic Republic of Congo. Based on morphological and molecular assessment of collections, we show that the species eaten by bonobos is a previously undescribed taxon described here as Hysterangium bonobo. This species is known in the local Bantu language (Bongando) as simbokilo and is used for baiting traps to catch several species of small mammals. Our findings highlight the need for further research into mycophagy and systematics of sequestrate fungi in Africa.

Jazz cats

Jazz cats

Investigating self-recognition in bonobos: mirror exposure reduces looking time to self but not unfamiliar conspecifics.

The question of whether animals have some sort of self-awareness is a topic of continued debate. A necessary precondition for self-awareness is the ability to visually discriminate the self from others, which has traditionally been investigated through mirror self-recognition experiments. Although great apes generally pass such experiments, interpretations of results have remained controversial. The aim of this study was to investigate how bonobos (Pan paniscus) respond to different types of images of themselves and others, both before and after prolonged mirror exposure. We first presented presumably mirror-naive subjects with representations of themselves in three different ways (mirror image, contingent and non-contingent video footage) as well as representations of others (video footage of known and unknown conspecifics). We found that subjects paid significantly less attention to contingent images of themselves (mirror image, video footage) than to non-contingent images of themselves and unfamiliar individuals, suggesting they perceived the non-contingent self-images as novel. We then provided subjects with three months of access to a large mirror centrally positioned in the enclosure. Following this manipulation, subjects showed significantly reduced interest in the non-contingent self-images, while interest in unknown individuals remained unchanged, suggesting that the mirror experience has led to a fuller understanding of their own self. We discuss implications of this preliminary investigation for the on-going debate on self-awareness in animals.

Differences in the mutual eye gaze of bonobos (Pan paniscus) and chimpanzees (Pan troglodytes).

Eye gaze is widespread in nonhuman primate taxa and important for social cognition and communicative signaling. Bonobos and chimpanzees, two closely related primate species, differ in social organization, behavior, and cognition. Chimpanzees' eye gaze and gaze following has been studied extensively, whereas less is known about bonobos' eye gaze. To examine species differences using a more ecologically relevant measure than videos or pictures, the current study compared bonobo and chimpanzee mutual eye gaze with a human observer. A multivariate analysis of variance revealed significant species differences in frequency and total duration, but not bout length, of mutual eye gaze (p < .001). Specifically, bonobos engage in mutual eye gaze more frequently and for longer total duration than chimpanzees. These results are likely related to species differences in social behavior and temperament and are consistent with eye-tracking studies in which bonobos looked at the eye region of conspecifics (in pictures and videos) longer than chimpanzees. Future research should examine the relationship between mutual eye gaze and gaze following, as well as examine its genetic and neurological correlates. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Occurrence and transmission of flu-like illness among neighboring bonobo groups at Wamba

Infectious diseases constitute one of the major threats to African great apes. Bonobos (Pan paniscus) may be particularly vulnerable to the transmission of infectious diseases because of their cohesive grouping and frequent social and sexual interactions between groups. Here we report two cases of a flu-like illness and possible transmission of the illness among neighboring wild bonobo groups at Wamba, DR Congo. The first flu-like outbreak started in the PE group on July 28, 2013, 2days after they had encounters with the BI and PW groups. All PE members, except for one infant, subsequently developed flu-like symptoms, including coughing and running nose. The second flu-like outbreak occurred in the E1 group on October 14, 2013, after E1 had encountered the PE group and the two groups stayed together from October 7 to 11. Eleven out of the 15 observed party members developed symptoms over the next 4days. The pathogens underlying the two outbreaks may have been related as two temporary immigrant females, who had previously shown symptoms while in the PE group, stayed briefly in the E1 group during the second outbreak, but did not show any symptoms.

Correction to: Genetic Analysis of Migration Pattern of Female Bonobos (Pan paniscus) Among Three Neighboring Groups

The original version of this article unfortunately contained mistakes. The changes are shown below:

Supplemental Material for Prior Experience Mediates the Usage of Food Items as Tools in Great Apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii)

Supplemental Material for Prior Experience Mediates the Usage of Food Items as Tools in Great Apes (Pan paniscus, Pan troglodytes, Gorilla gorilla, and Pongo abelii)

Recombination Between High-Risk Human Papillomaviruses and Non-Human Primate Papillomaviruses: Evidence of Ancient Host Switching Among Alphapapillomaviruses.

We use all the currently known 405 Papillomavirus (PV) sequences, 343 curated PV sequences from both humans and animals from the PAVE data base, to analyse the recombination dynamics of these viruses at the whole genome levels. After showing some evidence of human and non-human primate PV recombination, we report a comprehensive recombination analysis of all currently known 82 Alphapapillomaviruses (Alpha-PVs). We carried out an exploratory study and found novel recombination events between High-Risk HPV Types and Macaca fascicularis PV1 (MfPV1), Macaca Fuscata PV2 (MfuPV2) and Pan Paniscus PV1 (PpPV1) Papillomaviruses. This is the first evidence of interactions between PVs from different hosts and hence postulates the likelihood of ancient host switching among Alpha-PVs. Notwithstanding these results should be interpreted with caution because the major and minor parents indicated by RDP4 program are simply the sequences in the alignment that most closely resemble the actual parents. We found statistically significant differences between the phylogenies of the PV sequences with recombination regions and PV sequences without recombination regions using the Shimodaira–Hasegawa phylogenetic incongruence testing. We show that not more than 76MYA Alpha-PVs were in the same biological niche, a pre-requisite for recombination, and as the hosts evolved and diversified, the viruses adapted to specific host niches which eventually led to coevolution with specific hosts before speciation of primate species. Thus providing evidence that in ancient times no earlier than the Cretaceous period of the Mesozoic age, Alpha-PVs recombined and switched hosts, but whether this host switching is occurring currently is unknown. However, a clearer picture of the PVs evolutionary landscape can only be achieved with the incremental discovery of PV sequences, especially from the animal kingdom.Electronic supplementary materialThe online version of this article (10.1007/s00239-020-09946-0) contains supplementary material, which is available to authorized users.

No evidence of what-where-when memory in great apes (Pan troglodytes, Pan paniscus, Pongo abelii, and Gorilla gorilla).

Episodic memory is the ability to recollect specific past events belonging to our personal experience, and it is one of the most crucial human abilities, allowing us to mentally travel through time. In animals, however, evidence of what-where-when memory (hereafter, WWW memory) is limited to very few taxa, mostly reflecting the socioecological challenges faced in their environment. In this article, we aimed to replicate 2 studies previously conducted on birds and primates to find convincing evidence of WWW memory in great apes. For this purpose, we tested 12 captive great apes in 3 different tasks. In Task 1, we tested whether great apes take into account temporal information when choosing between highly preferred perishable and less-preferred nonperishable food items. In Task 2, we tested whether great apes can differentiate between similar events having happened at different times in the past. Finally, in Task 3, we tested whether great apes can use their memory flexibly, incorporating novel information in their memories. In none of the tasks did our subjects make the correct choice significantly above chance, with performance further declining when subjects were presented with 2 events (Task 2). Moreover, none of them could reliably integrate novel information into their memories. Overall, our study casts doubt on the existence of WWW memory in great apes, and especially calls for more caution when using WWW memory tasks and interpreting their results. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

The HLA A03 Supertype and Several Pan Species Major Histocompatibility Complex Class I A Allotypes Share a Preference for Binding Positively Charged Residues in the F Pocket: Implications for Controlling Retroviral Infections.

The major histocompatibility complex (MHC) class I region of humans, chimpanzees (Pan troglodytes), and bonobos (Pan paniscus) is highly similar, and orthologues of HLA-A, -B, and -C are present in both Pan species. Based on functional characteristics, the different HLA-A allotypes are classified into different supertypes. One of them, the HLA A03 supertype, is widely distributed among different human populations. All contemporary known chimpanzee and bonobo MHC class I A allotypes cluster genetically into one of the six HLA-A families, the HLA-A1/A3/A11/A30 family. We report here that the peptide-binding motif of the Patr-A*05:01 allotype, which is commonly present in a cohort of western African chimpanzees, has a strong preference for binding peptides with basic amino acids at the carboxyl terminus. This phenomenon is shared with the family members of the HLA A03 supertype. Based on the chemical similarities in the peptide-binding pocket, we inferred that the preference for binding peptides with basic amino acids at the carboxyl terminus is widely present among the human, chimpanzee, and bonobo MHC-A allotypes. Subsequent in silico peptide-binding predictions illustrated that these allotypes have the capacity to target conserved parts of the proteome of human immunodeficiency virus type 1 (HIV-1) and the simian immunodeficiency virus SIVcpz.IMPORTANCE Most experimentally infected chimpanzees seem to control an HIV-1 infection and are therefore considered to be relatively resistant to developing AIDS. Contemporary free-ranging chimpanzees may carry SIVcpz, and there is evidence for AIDS-like symptoms in these free-ranging animals, whereas SIV infections in bonobos appear to be absent. In humans, the natural control of an HIV-1 infection is strongly associated with the presence of particular HLA class I allotypes. The ancestor of the contemporary living chimpanzees and bonobos survived a selective sweep targeting the MHC class I repertoire. We have put forward a hypothesis that this may have been caused by an ancestral retroviral infection similar to SIVcpz. Characterization of the relevant MHC allotypes may contribute to understanding the shaping of their immune repertoire. The abundant presence of MHC-A allotypes that prefer peptides with basic amino acids at the C termini suggests that these molecules may contribute to the control of retroviral infections in humans, chimpanzees, and bonobos.

Investigating the Function of Mutual Grooming in Captive Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

Social grooming is often exchanged between individuals in many primate species. Rates of bidirectional (or simultaneous mutual) grooming vary across primate species, and its function is not yet fully understood. For example, mutual grooming is frequent in chimpanzees but rare in most primate species including wild bonobos. There are, however, no quantitative data available in captive bonobos. Therefore, through the direct comparison between captive bonobos and chimpanzees, this study aimed to (i) compare the frequency of mutual grooming between Pan species, (ii) explore and compare the function of mutual grooming, and (iii) discuss the rarity of this behavior in wild bonobo populations. We tested three hypotheses following the previous literature in wild chimpanzees. The social bonding hypothesis states that mutual grooming facilitates the maintenance of strong dyadic bonds. The immediate investment hypothesis states that it serves to signal willingness to invest in the interaction. The switching hypothesis states that mutual grooming serves no function but only occurs as an overlap to change the direction of unidirectional grooming. Our findings strongly supported the immediate investment hypothesis, but not the others. Grooming bouts that included mutual grooming were longer and more equitable than bouts without, illustrating that captive Pan species use mutual grooming to maximize their short-term benefits and increase the social value of their interaction. Captive bonobos performed mutual grooming in similar proportions and for similar functions as captive and wild chimpanzees do. This contrasts with wild bonobos who engage in this behavior only rarely. We suggest that the differences in patterns of mutual grooming between captive and wild bonobos might be explained by different degrees of kinship or by a potential intraspecies variation.

Correction to: Low Resistance of Senior Resident Females Toward Female Immigration in Bonobos (Pan paniscus) at Wamba, Democratic Republic of the Congo

Female aggression against outgroup conspecifics is an important aspect of intergroup relationships among female primates. Intense aggression from resident females toward immigrant females suggests that the costs of intrasexual competition outweigh the benefits of group living and has been reported in some species with female transfer. In bonobos (Pan paniscus), however, immigrant females are likely to integrate smoothly into an unfamiliar group through affiliative interactions with specific older females. We hypothesized that older resident females gain an indirect benefit from female immigration by increased mating opportunities for their philopatric sons. We examined the effects of 1) age and tenure and 2) the presence of adolescent or adult sons on the probability of aggression by resident females against immigrant females. We collected 73 instances of dyadic agonistic interactions between 14 female bonobos at Wamba, Democratic Republic of the Congo, for five different periods between November 2014 and June 2018, which included four immigrant females with a group tenure of <2.5 years. The female dominance hierarchy correlated with age and tenure, the slope of the hierarchy was weak but statistically significant, and the hierarchy was not linear. We found that the rate of aggression against immigrant females decreased with age in resident females but was unrelated to the presence of mature sons. Our findings suggest that the cost imposed by female immigration varies among resident females, and that social tolerance to immigrant females may be associated with low feeding competition rather than any future benefits.

Drawn out of the shadows: Surveying secretive forest species with camera trap distance sampling

Abstract With animal species disappearing at unprecedented rates, we need an efficient monitoring method providing reliable estimates of population density and abundance, critical for the assessment of population status and trend. We deployed 160 camera traps (CTs) systematically over 743 locations covering 17,127 km2 of evergreen lowland rainforest of Salonga National Park, block South, Democratic Republic of the Congo. We evaluated the applicability of CT distance sampling (CTDS) to species different in size and behaviour. To improve precision of estimates, we evaluated two methods estimating species' availability (‘A’) for detection by CTs. We recorded 16,700 video clips, revealing 43 different animal taxa. We estimated densities of 14 species differing in physical, behavioural and ecological traits, and extracted species‐specific availability from available video footage using two methods (a) ‘ACa’ (Cappelle et al. [2019] Am. J. Primatol., 81, e22962) and (b) ‘ARo’ (Rowcliffe et al. [2014] Methods Ecol. Evol. 5, 1170). With sample sizes being large enough, we found minor differences between ACa and ARo in estimated densities. In contrast, low detectability and reactivity to the camera were main sources of bias. CTDS proved efficient for estimating density of homogenously rather than patchily distributed species. Synthesis and applications. Our application of camera trap distance sampling (CTDS) to a diverse vertebrate community demonstrates the enormous potential of this methodology for surveys of terrestrial wildlife, allowing rapid assessments of species' status and trends that can translate into effective conservation strategies. By providing the first estimates of understudied species such as the Congo peafowl, the giant ground pangolin and the cusimanses, CTDS may be used as a tool to revise these species' conservation status in the IUCN Red List of Threatened Species. Based on the constraints we encountered, we identify improvements to the current application, enhancing the general applicability of this method.

Mandibular corpus shape is a taxonomic indicator in extant hominids

The aim of this study is to understand whether the shape of three sub-regions of the mandibular corpus (the alveolar arch, corpus at M1 and posterior symphysis) are useful for making taxonomic assessments at the genus and species levels in extant hominids. We use data taken from 3D surface scans of the mandibular corpus of seven extant hominid taxa: Gorilla gorilla gorilla, Gorilla beringei graueri, Homo sapiens, Pan paniscus, Pan troglodytes schweinfurthii, Pongo abelii, and Pongo pygmaeus pygmaeus to generate four shape variables: alveolar arch shape (AAS), corpus shape at M1 (CSM1 ), posterior symphysis shape at the midline (PSSM), and posterior symphysis shape (PSS). To ascertain how reliable each mandibular shape variable is for assessing taxonomy, we ran canonical discriminant and discriminant function analysis, reporting cross-validated results. Using a combination of three mandibular corpus shape variables, 99% of specimens were classified correctly for genus-level analyses. A maximum of 100% of Pan specimens, 94% of Gorilla specimens and 96% of Pongo specimens were classified correctly at the species level when up to three mandibular shape variables were included in the analyses. When mandibular corpus variables were considered in isolation, posterior symphysis shape yielded the highest overall correct classification results. The high taxonomic classification rates at both the genus and species level, using 3D surface data and advanced quantification techniques, show that the shape of the alveolar arch, corpus at M1 and symphysis can distinguish extant hominid taxa. These findings have implications for assessing the taxonomy of extinct hominid specimens which preserve these mandibular sub-regions.

Metacarpophalangeal joint loads during bonobo locomotion: model predictions versus proxies.

The analysis of internal trabecular and cortical bone has been an informative tool for drawing inferences about behaviour in extant and fossil primate taxa. Within the hand, metacarpal bone architecture has been shown to correlate well with primate locomotion; however, the extent of morphological differences across taxa is unexpectedly small given the variability in hand use. One explanation for this observation is that the activity-related differences in the joint loads acting on the bone are simply smaller than estimated based on commonly used proxies (i.e. external loading and joint posture), which neglect the influence of muscle forces. In this study, experimental data and a musculoskeletal finger model are used to test this hypothesis by comparing differences between climbing and knuckle-walking locomotion of captive bonobos (Pan paniscus) based on (i) joint load magnitude and direction predicted by the models and (ii) proxy estimations. The results showed that the activity-related differences in predicted joint loads are indeed much smaller than the proxies would suggest, with joint load magnitudes being almost identical between the two locomotor modes. Differences in joint load directions were smaller but still evident, indicating that joint load directions might be a more robust indicator of variation in hand use than joint load magnitudes. Overall, this study emphasizes the importance of including muscular forces in the interpretation of skeletal remains and promotes the use of musculoskeletal models for correct functional interpretations.

Altruistic food sharing behavior by human infants after a hunger manipulation

Altruistic behavior entails giving valuable benefits to others while incurring a personal cost. A distinctively human form of altruistic behavior involves handing nutritious food to needy strangers, even when one desires the food. Engaging in altruistic food transfer, instead of keeping the food, is costly, because it reduces the caloric intake of the benefactor vis-à-vis the beneficiary. Human adults engage in this form of altruistic behavior during times of war and famine, when giving food to others threatens one’s own survival. Our closest living primate relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), exhibit notable constraints on the proclivity to engage in such food transfer (particularly chimpanzees), although they share many social-cognitive commonalities with humans. Here we show that in a nonverbal test, 19-month-old human infants repeatedly and spontaneously transferred high-value, nutritious natural food to a stranger (Experiment 1) and more critically, did so after an experimental manipulation that imposed a feeding delay (Experiment 2), which increased their own motivation to eat the food. Social experience variables moderated the expression of this infant altruistic behavior, suggesting malleability.

Impressive Arboreal Gap-Crossing Behaviors in Wild Bonobos, Pan paniscus

Most primates are arboreal, and the current context of habitat fragmentation makes gap- and road-crossing behaviors more and more common. Great apes may try to avoid behaviors such as arboreal leaping because given their size such behaviors are risky. Here, we report impressive gap-crossing by wild bonobos (Pan paniscus) in the Democratic Republic of Congo, induced by human disturbance and habitat fragmentation. We quantify the basic mechanics of leaps and arboreal landing performance in two individuals. The bonobos climbed a tree, 15 m high, and performed pronograde leaps between thin flexible branches, to grasp landing branches ca. 4 m further and below their starting point. They reached an instantaneous velocity of about 9 m · s−1. The bonobos used pendular swinging of landing branches to dissipate the kinetic energy built up during falling, requiring a grip force of about 2.5× body weight. Moreover, our results show that bonobos might be able to modulate the drag experienced during falling (up to 20% of body weight) by adjusting their posture. Apparently, bonobos evaluate the structural context to perform the best possible leap and balance the risks against the extra energetic costs involved. Further study of locomotor performance is needed to inform conservation planning, owing to the extent of habitat fragmentation due to human activities.

Predicting body mass of bonobos (Pan paniscus) with human-based morphometric equations.

A primate's body mass covaries with numerous ecological, physiological, and behavioral characteristics. This versatility and potential to provide insight into an animal's life has made body mass prediction a frequent and important objective in paleoanthropology. In hominin paleontology, the most commonly employed body mass prediction equations (BMPEs) are "mechanical" and "morphometric": uni- or multivariate linear regressions incorporating dimensions of load-bearing skeletal elements and stature and living bi-iliac breadth as predictor variables, respectively. The precision and accuracy of BMPEs are contingent on multiple factors, however, one of the most notable and pervasive potential sources of error is extrapolation beyond the limits of the reference sample. In this study, we use a test sample requiring extrapolation-56 bonobos (Pan paniscus) from the Lola ya Bonobo sanctuary in Kinshasa, Democratic Republic of the Congo-to evaluate the predictive accuracy of human-based morphometric BMPEs. We first assess systemic differences in stature and bi-iliac breadth between humans and bonobos. Due to significant differences in the scaling relationships of body mass and stature between bonobos and humans, we use panel regression to generate a novel BMPE based on living bi-iliac breadth. We then compare the predictive accuracy of two previously published morphometric equations with the novel equation and find that the novel equation predicts bonobo body mass most accurately overall (41 of 56 bonobos predicted within 20% of their observed body mass). The novel BMPE is particularly accurate between 25 and 45 kg. Given differences in limb proportions, pelvic morphology, and body tissue composition between the human reference and bonobo test samples, we find these results promising and evaluate the novel BMPE's potential application to fossil hominins.

Low Resistance of Senior Resident Females Toward Female Immigration in Bonobos (Pan paniscus) at Wamba, Democratic Republic of the Congo

Female aggression against outgroup conspecifics is an important aspect of intergroup relationships among female primates. Intense aggression from resident females toward immigrant females suggests that the costs of intrasexual competition outweigh the benefits of group living and has been reported in some species with female transfer. In bonobos (Pan paniscus), however, immigrant females are likely to integrate smoothly into an unfamiliar group through affiliative interactions with specific older females. We hypothesized that older resident females gain an indirect benefit from female immigration by increased mating opportunities for their philopatric sons. We examined the effects of 1) age and tenure and 2) the presence of adolescent or adult sons on the probability of aggression by resident females against immigrant females. We collected 73 instances of dyadic agonistic interactions between 14 female bonobos at Wamba, Democratic Republic of the Congo, for five different periods between November 2014 and June 2018, which included four immigrant females with a group tenure of <2.5 years. The female dominance hierarchy correlated with age and tenure, the slope of the hierarchy was weak but statistically significant, and the hierarchy was not linear. We found that the rate of aggression against immigrant females decreased with age in resident females but was unrelated to the presence of mature sons. Our findings suggest that the cost imposed by female immigration varies among resident females, and that social tolerance to immigrant females may be associated with low feeding competition rather than any future benefits.

Supplemental Material for Differences in the Mutual Eye Gaze of Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

Supplemental Material for Differences in the Mutual Eye Gaze of Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)