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One of the current threats to the bonobo (Pan paniscus), a highly endangered ape species only found in the Democratic Republic of the Congo, are anthropozoonoses caused by human respiratory viruses. To date, epidemiological information regarding respiratory viral infections in bonobos is limited. In this study, we examined fecal immunoglobulin A antibodies against human respiratory viruses in bonobos, which may help estimating the viral prevalence. A substantial proportion of bonobos were positive for the antiviral antibodies, including those against parainfluenza virus, respiratory syncytial virus, influenza virus, rhinovirus, and mumps virus. The prevalence of the antibodies was found to depend on the viral species and bonobo populations, suggesting that the bonobos had been exposed to these respiratory viruses. These results may indicate the need for an epidemiological evidence-based action plan for the protection of bonobos from anthropozoonoses.

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, 2 days 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 4 days. 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.

One of the current threats to the bonobo (Pan paniscus), a highly endangered ape species only found in the Democratic Republic of the Congo, are anthropozoonoses caused by human respiratory viruses. To date, epidemiological information regarding respiratory viral infections in bonobos is limited. In this study, we examined fecal immunoglobulin A antibodies against human respiratory viruses in bonobos, which may help estimating the viral prevalence. A substantial proportion of bonobos were positive for the antiviral antibodies, including those against parainfluenza virus, respiratory syncytial virus, influenza virus, rhinovirus, and mumps virus. The prevalence of the antibodies was found to depend on the viral species and bonobo populations, suggesting that the bonobos had been exposed to these respiratory viruses. These results may indicate the need for an epidemiological evidence-based action plan for the protection of bonobos from anthropozoonoses.

Intergroup interactions in primates vary from nonagonistic to severely aggressive. Food resources and fertile females cause intergroup aggression when groups defend resources and mates from other groups. Peaceful intermingling during intergroup encounters is rare but has been reported in several primates, including bonobos (Pan paniscus). Although intergroup encounters in bonobos occur at both nonprovisioned and provisioned sites, provisioning may be one factor responsible for frequent intergroup encounters. We studied intergroup encounters between one bonobo group (PE) and its neighboring groups, one semihabituated and two habituated groups, under nonprovisioned conditions in 2010–2015 at Wamba, Democratic Republic of Congo. We examined whether fruit abundance and females with sexual swellings influenced encounter frequency. PE group encountered the other groups on 7.1 days (mean, range: 0–19) per month. Up to four different groups met simultaneously at one location. Encounter frequency was highest around the yearly peak in fruit abundance, suggesting that reduced food competition is linked to increased encounter frequency. During periods of relatively low fruit abundance, the probability of an encounter was higher when a higher number of adult females with maximum sexual swellings were present, suggesting that the attractiveness of females with sexual swellings promoted group encounters during periods of relatively low fruit abundance. These findings suggest that both competition for food and the availability of females with sexual swellings influence encounter frequency in bonobos.

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, 2 days 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 4 days. 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.

In many group-living mammals, mothers may increase the reproductive success of their daughters even after they are nutritionally independent and fully grown [1]. However, whether such maternal effects exist for adult sons is largely unknown. Here we show that males have higher paternity success when their mother is living in the group at the time of the offspring’s conception in bonobos (N = 39 paternities from 4 groups) but not in chimpanzees (N = 263 paternities from 7 groups). These results are consistent with previous research showing a stronger role of mothers (and females more generally) in bonobo than chimpanzee societies. Postprint Postprint

OBJECTIVES Although conflicts between groups over valuable resources are common in the animal kingdom, an individual's strategy toward out-group individuals may differ according to the benefits and costs received from inter-group interactions. Groups of bonobos encounter each other frequently and may mingle and range together from a few hours to a few days. During these inter-group associations, individuals across groups exhibit both aggressive and affiliative interactions. This study aimed to examine the strategies that bonobos employ with other groups, by comparing the patterns of within- and inter-group aggression. MATERIALS AND METHODS We observed the aggressive interactions within a group of wild bonobos and between the group and three neighboring groups in Wamba, Luo Scientific Reserve, DR Congo. RESULTS Bonobos increased the level of cooperation to attack out-group individuals more than they do to attack within-group individuals. Additionally, they reduced the aggression between within-group members during inter-group associations, compared to that when not associated with other groups. Males selectively and cooperatively attacked out-group males. Inter-group aggression among females was rare. Furthermore, females sometimes formed coalitions with out-group individuals to attack a common target. DISCUSSION Our results support the hypothesis that inter-group competition occurs in bonobos, with males across groups competing over mates. Females across groups were tolerant and even cooperative with each other. Regardless of the ideal male strategy, female tolerant and cooperative relationships across groups and female within-group superiority over males could preserve tolerant inter-group relationships in bonobos.

Maternal cannibalism, whereby a mother consumes her own offspring, occurs in various animal taxa and is commonly explained by nutritional stress or environmental pressures. It is rare in nonhuman primates and is considered an aberrant behavior only observed under high-stress conditions. It was therefore surprising when, in the first reported case of cannibalism in wild bonobos, a mother consumed part of the dead infant at LuiKotale. Here we report two more cases of maternal cannibalism by wild bonobos at two different study sites, Wamba and Kokolopori. The dead infants' mothers participated in the cannibalism in both cases. At Kokolopori, although the mother did consume part of the carcass, it was held and shared by another dominant female. At Wamba, the mother was a dominant female within the community and was the primary consumer of the carcass. In both cases, cannibalism resembled other meat-eating events, with the dominant female controlling meat consumption. Infanticide was not observed in either case, but its occurrence could not be ruled out. Although rare, the occurrence of maternal cannibalism at three different study sites suggests that this may represent part of the behavioral repertoire of bonobos, rather than an aberrant behavior.

Patterns of coalitionary aggression among female animals are generally explained by kin selection theory. Frequent female coalitions are almost exclusively observed in female-philopatric species, where females stay in their natal group, and females typically form coalitions with their kin. Bonobos, Pan paniscus , in contrast, are male-philopatric, with females emigrating to new groups at adolescence, but female bonobos frequently form coalitions even though they are generally with nonrelatives. Here we investigated the patterns of female coalitions in a group of wild bonobos at Wamba, Democratic Republic of the Congo, in order to explore alternative mechanisms to kin selection for cooperation among females. We found that all female coalitions (defined as coalitions in which two or more females participated) were formed to attack males, usually after the male(s) behaved aggressively towards one or more females. There was no evidence that female bonobos used proximity, grooming or genito-genital rubbing (GG-rubbing) to develop coalition partnerships, although higher association provided females with more opportunity to form coalitions. Instead of reciprocal agonistic support, we found a unidirectional pattern in which older females supported younger females. Females defeated males more easily when they formed coalitions than when they confronted males alone. Unlike female coalitions in other species that use coalitions to cope with competition among females, our results suggest that coalitions in female bonobos might have evolved as a counterstrategy against male harassment. Females might choose their coalition partners based not on affiliative relationship or reciprocity but on mutualism. In contrast to the hypothesis that affiliative behaviour leads to coalition formation, coalitions might in fact increase gregariousness among females, leading females to develop affiliative interactions that promote tolerance.

One of the most conspicuous behavioural differences among great apes is the paucity of tool use among wild bonobos (Pan paniscus) in comparison to chimpanzees (Pan troglodytes) who are one of the most prolific and skilled tool users in the animal kingdom. This is in spite of the fact that bonobo tool use repertories are as large and diverse as chimpanzees’ in captive settings. In this study, we compared tool using behaviours and potential drivers of these behaviours in the Wamba bonobo population located in central Democratic Republic of Congo with the Goualougo chimpanzee population of northern Republic of Congo. The tool use repertoire of wild bonobos was comprised of only 13 behaviours, compared to 42 for chimpanzees. However, the number of tool behaviours observed in each study site was similar between bonobos and chimpanzees, and many types of tool use for social, self-grooming/stimulation, and comfort/protection functions were commonly used by both species. A marked difference is that 25 of 42 tool behaviours exhibited by chimpanzees are performed for feeding, in contrast to a single report of bonobos using a leaf sponge to drink water. We examined whether the differences in tool use repertoires can be explained by the necessity, opportunity, relative profitability, or invention hypotheses. We found that habitat composition and fluctuation of fruit production at these two sites were similar, particularly when compared with variation observed between sites within each species. Thus it was unlikely that the necessity hypothesis explains the lack of tool use for feeding in bonobos. Though further study at Wamba is needed, we did not identify any obvious differences in prey availability that would indicate differences in tool using opportunities between the sites. This study could not test the relative profitability hypothesis, and further research is needed on whether tool use is the most efficient means of calorie or protein intake for wild apes. Bonobos at Wamba formed much larger and stable parties than chimpanzees at Goualougo, which was contrary to the prediction by the invention hypothesis. Another explanation is that differences in tool use behaviour between bonobos and chimpanzees might not be explained by the current ecological or social conditions, but rather by circumstances during the Pleistocene Epoch. The observed species differences might also reflect divergent behavioural predispositions, rather than actual differences in cognitive abilities.

We report here where the most recent common ancestor (MRCA) of bonobos (Pan paniscus) ranged and how they dispersed throughout their current habitat. Mitochondrial DNA (mtDNA) molecular dating to analyze the time to MRCA (TMRCA) and the major mtDNA haplogroups of wild bonobos were performed using new estimations of divergence time of bonobos from other Pan species to investigate the dispersal routes of bonobos over the forest area of the Congo River’s left bank. The TMRCA of bonobos was estimated to be 0.64 or 0.95 million years ago (Ma). Six major haplogroups had very old origins of 0.38 Ma or older. The reconstruction of the ancestral area revealed the mitochondrial ancestor of the bonobo populations ranged in the eastern area of the current bonobos’ habitat. The haplogroups may have been formed from either the riparian forests along the Congo River or the center of the southern Congo Basin. Fragmentation of the forest refugia during the cooler periods may have greatly affected the formation of the genetic structure of bonobo populations.

Group-living animals need to coordinate their activity in order to maintain gregariousness. Although individuals have their own nutritional, social, and reproductive needs, they have to reach consensus to decide where and when to travel. Collective movements are the outcome of one individual’s departure, who is then followed by other group members. We investigated departure initiation in a group of bonobos at Wamba, DR Congo, to determine the distribution of leadership among group members. If three or more bonobos started moving more than 30 m, we assigned the individual who moved first as the one who initiated the movement. Two hundred and fifty-four departures were observed. First, we examined whether the frequency of initiation differed according to the following attributes of individuals: sex, age, stage in sexual swelling cycle, dominance, and affiliative relationship. We also examined whether one or more individual(s) initiate departure more or less frequently than expected by chance. A significant interaction between sex and age was found, indicating that the effect of age was greater among females than among males. Individuals who were more central to the grooming network initiated departures more frequently. The three oldest females initiated more often than expected. Old females may be followed because of coalitionary supports they often give to younger females, and of their greater knowledge about ranging area. Leadership in bonobos was not equally shared among group members, and old females were “key individuals” who helped to maintain cohesiveness in their fission-fusion society. When group-living animals travel from one location to another, they must coordinate when and where to travel; otherwise, they might spread apart. Bonobos are one of our closest living relatives and have a fission-fusion social system. We investigated the initiation of group departure in wild bonobos to determine the distribution of leadership among group members. We found that the frequency of initiation was associated with the individual’s age, affiliative relationships, and male dominance rank. The three oldest females initiated departures more frequently than expected, suggesting that these individuals were habitual initiators and took an important role to preserve cohesiveness. We discuss how this “old female leadership” may emerge in a male-philopatric society.

This is the first report to demonstrate that a large mixed-sex party of bonobos travelled a long distance to return to the location of a snare apparently to search for a member that had been caught in it. An adult male was caught in a metallic snare in a swamp forest at Wamba, Luo Scientific Reserve, Democratic Republic of the Congo. After he escaped from the snare by breaking a sapling to which the snare was attached, other members of his party assisted him by unfastening the snare from lianas in which it was caught and licked his wound and tried to remove the snare from his fingers. In the late afternoon, they left him in the place where he was stuck in the liana and travelled to the dry forest where they usually spend the night. The next morning, they travelled back 1.8 km to revisit the location of the injured male. When they confirmed that he was no longer there, they returned to the dry forest to forage. This was unlike the usual ranging patterns of the party, suggesting that the bonobos travelled with the specific intention of searching for this injured individual who had been left behind. The incident described in this report likely occurred because bonobos usually range in a large mixed-sex party and try to maintain group cohesion as much as possible.

International audience; This paper first reviews data collected from 1976 to 2013 regarding the life histories of members of the main E1 study group of bonobos (Pan paniscus) in Wamba. The E1 group exhibited strong tendencies toward female dispersal and male residence during the entire study period, thereby exemplifying the typical characteristics of a male-philopatric and female-dispersal society. This pattern did not change after the abandonment of artificial provisioning. We then present two new cases of immigrant females, focusing especially on social association patterns, dominance relationships, and affiliative interactions during the approximate 2.5 years from the time of their immigration to their first birth. These females began engaging in social grooming with resident females immediately after their arrival but rarely did so with adult males, suggesting that they regard social bonding with females as more important than that with males. They also emigrated at a young age and frequently engaged in social play. Indeed, social bonding established through frequent social play may be related to the development of socially symmetrical relationships, which are the basis for the egalitarian bonobo society. Intragroup competition for food and mates was unlikely explanations for the tendency toward female dispersal. However, male residence and the risk of father–daughter incest may encourage female transfer among 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.

Bonobos (Pan paniscus) inhabit regions south of the Congo River including all areas between its southerly tributaries. To investigate the genetic diversity and evolutionary relationship among bonobo populations, we sequenced mitochondrial DNA from 376 fecal samples collected in seven study populations located within the eastern and western limits of the species' range. In 136 effective samples from different individuals (range: 7-37 per population), we distinguished 54 haplotypes in six clades (A1, A2, B1, B2, C, D), which included a newly identified clade (D). MtDNA haplotypes were regionally clustered; 83 percent of haplotypes were locality-specific. The distribution of haplotypes across populations and the genetic diversity within populations thus showed highly geographical patterns. Using population distance measures, seven populations were categorized in three clusters: the east, central, and west cohorts. Although further elucidation of historical changes in the geological setting is required, the geographical patterns of genetic diversity seem to be shaped by paleoenvironmental changes during the Pleistocene. The present day riverine barriers appeared to have a weak effect on gene flow among populations, except for the Lomami River, which separates the TL2 population from the others. The central cohort preserves a high genetic diversity, and two unique clades of haplotypes were found in the Wamba/Iyondji populations in the central cohort and in the TL2 population in the eastern cohort respectively. This knowledge may contribute to the planning of bonobo conservation.