Tetsuya Sakamaki

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.

Long-Term Studies on Wild Bonobos at Wamba, Luo Scientific Reserve, D. R. Congo: Towards the Understanding of Female Life History in a Male-Philopatric Species

Long-term studies on wild bonobos began at Wamba, in the current Luo Scientific Reserve, in 1973. Except for several interruptions due to political instability and civil war, we have been conducting studies of identified individual bonobos over 35 years, providing valuable data on their population dynamics and life history. Although the number of groups and number of individuals in the northern section of the reserve decreased by half during the interruptions of the study, the number of members of the main study group has steadily increased since 2002 when we resumed the study. Our long-term data demonstrated the male-philopatric structure of the group. There is no confirmed case of emigration of males from the study group, and no case of immigration of males into the group. On the other hand, all females born into the study group disappeared by the age of 10 years, and females with estimated ages of 6–13 years immigrated into the study group. These ages of intergroup transfer are much earlier than those reported for chimpanzees. Exceptional cases of immigration of two adult males and two adult females with offspring occurred right after the war. It is likely that remnants of extinct groups joined the study group. Such integration of members of foreign groups highlights the peaceful nature of bonobo society. The study group is characterized by an extremely high tendency for female aggregation. Various factors, including high density of food patches, female initiative in ranging, prolonged estrus of females, and high social status of females, seem to be responsible for the high attendance ratio of females in mixed-sex parties. Our long-term observations therefore provided evidence for interesting behavioral contrasts with chimpanzees.

An Attempted Within-group Infanticide in Wild Chimpanzees

Two high-ranking adult male chimpanzees (Pan troglodytes) of M group in the Mahale Mountains National Park, Tanzania, tried to get a newborn female infant of an adult female who was born in M group. The mother was not seen to mate with these adult males during the probable conception cycle of the infant, but she disappeared from the group during the later cycle, when she may have been inseminated by a male of one of the neighboring unit groups. The adult males failed to get the infant because the grandmother of the newborn and her female friend cooperated to protect the mother and infant from attacks by the males. The sexual selection hypothesis for infanticide by adult male chimpanzees holds for this observed case. The sudden disappearance of another infant, a healthy female, strongly suggests the killing of female infants too. Therefore, the asserted male-biased infanticide in chimpanzees appears to be less tenable.

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.

Adult hookworms (Necator spp.) collected from researchers working with wild western lowland gorillas.

BackgroundIn general, studies on the diversity of strongylid nematodes in endangered host species are complicated as material obtained by non-invasive sampling methods has limited value for generic and species identification. While egg morphology barely allows assignment to family, the morphology of cultivated infective third stage larvae provides a better resolution at the generic level but cannot be used for exact species identification. Morphology-based taxonomic approaches greatly depend on the examination of adult worms that are usually not available.MethodsHookworm parasites in two European researchers, who participated in gorilla research in the Central African Republic, were expelled after anthelmintic treatment to the faeces, collected and morphologically examined. A male worm discharged naturally from a wild bonobo (Pan paniscus) in Congo was also examined for comparison.ResultsTwo species of Necator were identified in researchers’ faecal material: Necator americanus (Stiles, 1902) and N. gorillae Noda & Yamada, 1964; the latter species differed in having a smaller body, smaller buccal cavity and shorter spicules with spade-shaped membranes situated distally. Males of N. gorillae also possessed unusual cuticular thickenings on the dorsal side of the prebursal region of the body. These characters, shared with the male worm from the bonobo, correspond well to the description of N. gorillae described from gorillas in Congo.ConclusionsBased on the morphology of the hookworms recovered in this study and previous molecular analyses of larvae developed from both humans and western lowland gorillas (Gorilla gorilla gorilla) from this locality, we conclude that the researchers became infected with gorilla hookworms during their stay in the field. This is the first report of infection with a Necator species other than N. americanus in humans.

Habitat use of bonobos (Pan paniscus) at Wamba: Selection of vegetation types for ranging, feeding, and night‐sleeping

Understanding the habitat requirements of great apes is essential for effective conservation strategies. We examined annual habitat use of a bonobo group in the Wamba field site within the Luo Scientific Reserve, Democratic Republic of the Congo. Using satellite imagery, we categorized the groups ranging area into three forest types: (1) primary and old secondary forest (P/OS), (2) young secondary forest and agriculture (YS/Ag), and (3) swamp forest (Sw). We tracked the group for 1 year (2007–2008) and compared usage of the three forest types for ranging, feeding, and night‐sleeping. We also recorded what the bonobos ate and monitored monthly fruit availability in each forest type. The group ranged and fed more often in P/OS and less often in YS/Ag and Sw than expected based on habitat availability. Also, the group slept mostly in P/OS (94% of nights monitored), but also in YS/Ag (1%), and Sw (5%). Fruit availability in P/OS had no significant effect on habitat selection, but the group fed in YS/Ag most often during the two months when fruits in P/OS were least abundant. In June, when fruit of Uapaca spp. (selectively eaten by bonobos) was generally abundant in Sw, the group mostly ranged and slept there. The bonobos fed most often on herbaceous plants in all three forest types. In Sw, the bonobos frequently ate mushrooms. Our results show that semi‐open forest with abundant herbaceous plants such as YS/Ag could be an important feeding habitat and may provide fallback food for bonobos when fruits are scarce. Furthermore, Sw can serve seasonally as a main habitat to complement P/OS if adequate food resources and tree nesting opportunities are available. We conclude that bonobos use diverse habitats depending on their needs and we highlight the importance of minor‐use habitats for sustaining populations of target species in conservation planning. Am. J. Primatol. 77:701–713, 2015.

Social grooming among wild bonobos (Pan paniscus) at Wamba in the Luo Scientific Reserve, DR Congo, with special reference to the formation of grooming gatherings

Chimpanzees (Pan troglodytes) groom in gatherings in which many individuals may be connected via multiple chains of grooming and they often exchange partners with each other. They sometimes groom another while receiving grooming; that is, one animal can play two roles (i.e., groomer and groomee) simultaneously. Although this feature of chimpanzees is notable from the viewpoint of the evolution of human sociality, information on our other closest living relative, the bonobo (Pan paniscus), is still lacking. In this study, I describe grooming interactions of bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo (DR Congo), with a particular focus on the formation of grooming gatherings. Like chimpanzees, the bonobos also performed mutual grooming (two individuals grooming each other simultaneously) and polyadic grooming (three or more individuals). However, unlike chimpanzees, these sessions lasted for only a short time. Bonobos rarely groomed another while receiving grooming. Because social grooming occurred not only in trees but also in open spaces, including treefall gaps, the conditions did not necessarily limit the opportunity to make multiple chains of grooming. However, bonobos also engaged in social grooming in different ways from chimpanzees; That is, many individuals were involved simultaneously at a site, in which they separated for dyadic grooming. Some cases clearly showed that bonobos preferred a third party not to join while grooming in a dyad, suggesting that bonobos have a preference for grooming in dyads and that immature individuals formed the preference that was shared among adults while growing up. Most members of the study group ranged together during the majority of the study period. Although bonobos show a fission–fusion grouping pattern, when group members frequently encounter one another on a daily basis, they may not be motivated to form multiple grooming chains at this site, as do chimpanzees.

A New Code of Observation Employed at Mahale: Prevention against a Flu-like Disease

Associate Editors: Christophe Boesch, Max-Planck Institute, Germany Jane Goodall, Jane Goodall Institute, USA Takayoshi Kano, Kyoto University, Japan Tetsuro Matsuzawa, Kyoto University, Japan William C. McGrew, University of Cambridge, UK John C. Mitani, University of Michigan, USA Vernon Reynolds, Budongo Forest Project, UK Yukimaru Sugiyama, Kyoto University, Japan Richard W. Wrangham, Harvard University, USA

Paternity and kin structure among neighbouring groups in wild bonobos at Wamba

Although both bonobos and chimpanzees are male-philopatric species, outcomes of male–male reproductive competition seem to be more closely associated with mating success in chimpanzees. This suggests that the extent of male reproductive skew is lower in bonobos. In addition, between-group male–male reproductive competition is more lethal in chimpanzees. This suggests that between-group differentiation in male kinship is lower in bonobos. We analysed the paternity of 17 offspring in two bonobo groups and estimated the relatedness of individuals among three neighbouring groups by using DNA extracted from non-invasive samples at Wamba, in the Democratic Republic of the Congo. The alpha males sired at least nine of 17 offspring. This supports a previous finding that the male reproductive skew is higher in bonobos than that in chimpanzees. Average relatedness among males within groups was significantly higher than that among males across groups, whereas there was no significant difference among females between within and across groups. These results are consistent with male philopatry, highly skewed reproductive success of males and female dispersal. Higher average relatedness among males within groups suggest that the differences in hostility towards males of different groups between bonobos and chimpanzees may be explained by factors other than kinship.