Nahoko Tokuyama

Genetic Structure of Wild Bonobo Populations: Diversity of Mitochondrial DNA and Geographical Distribution

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.

Why do wild bonobos not use tools like chimpanzees do

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.

Do friends help each other? Patterns of female coalition formation in wild bonobos at Wamba

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.

Intergroup Transfer of Females and Social Relationships Between Immigrants and Residents in Bonobo (Pan paniscus) Societies

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.

Cases of maternal cannibalism in wild bonobos (Pan paniscus) from two different field sites, Wamba and Kokolopori, Democratic Republic of the Congo

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.

Redirected aggression reduces the cost for victims in semi-provisioned free-ranging Japanese macaques (Macaca fuscata fuscata)

In many social species, the victim often attacks an uninvolved third individual soon after a conflict. This behaviour is called ‘redirected aggression’ or ‘redirection’, and its role(s) remain(s) controversial. We observed semi-provisioned free-ranging Japanese macaques at Iwatayama Monkey Park in Arashiyama, Kyoto, Japan, to test three hypotheses concerning the function of redirected aggression: Japanese macaques perform redirection to (1) indirectly retaliate against the aggressor, (2) reduce post-conflict stress, or (3) reduce post-conflict uncertainty. When we observed aggressive interactions, we recorded the behaviour of victims during the subsequent 10 min. Redirection occurred more frequently when the rank of the victim of the initial conflict was high, when the victim was an older monkey, and when conflicts occurred among kin. The results largely supported hypothesis 3. Victims received renewed aggression not only from the initial aggressor but also from bystanders more frequently within 1 min after the initial conflict than in the subsequent 9 min. Victims who performed redirection received less aggression from bystanders. Victims might have been able to avoid renewed aggression because they could change their state from victim to aggressor by performing redirection. This effect of redirection did not differ with the victim’s rank. However, the lower the victim’s rank, the higher the risk that they would receive retaliation from the target of the redirected aggression or the latter’s kin. Thus, redirection caused the same magnitude of benefit and a different magnitude of risk according to the victim’s rank. The victim may need to judge his/her own situation when making the decision as to whether to perform redirection.

The mitochondrial ancestor of bonobos and the origin of their major haplogroups

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.

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.