Partner choice in genito-genital rubbing among female bonobos (Pan paniscus) is highly dependent on physical proximity.

Sociosexual interactions of non-human primates have multiple functions, and information on partner choice could help us to determine the major purpose of these behaviors. Female bonobos (Pan paniscus) frequently engage in genito-genital (GG) rubbing, which is categorized as a sociosexual behavior. The functions of GG rubbing may vary across allopatric bonobo populations, especially in relation to its use in social bonding. Thus, we aimed to examine the use of GG rubbing in the formation and maintenance of social bonds by examining partner choice in this context in the habituated bonobo population at Wamba, Democratic Republic of the Congo. We examined the effect of female age (and correlated dominance rank) on the proportion of solicited GG rubbing, and the effects of age difference, proximity index, and grooming index on the successful GG rubbing occurrences. Our results showed that female age significantly affected the proportion of solicited GG rubbing, indicating that older and higher-ranking females solicited this activity more frequently. Individuals of female-female dyads who were close in age and dominance rank frequently engaged in GG rubbing. The more the females in a dyad were in physical proximity, the more they engaged in GG rubbing. No correlation was observed between grooming and GG rubbing. These results indicate that partner choice in GG rubbing is highly dependent on physical proximity, and suggest that characteristics of female gregariousness might be important with respect to this choice among bonobos.

Bonobo social organization at the seasonal forest-savanna ecotone of the Lomami national park.

Examining the relationship between food and primate social organization helps us understand how the environment shaped hominin social evolution. However, there is debate as to whether the social differences between our two closest relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes), are due to differences in food availability between their respective habitats or to nonenvironmental factors. The most prominent theory is that bonobo communities have more socially cohesive, stable parties, centered on gregarious females because they evolved in food-rich habitat where individuals, especially females, are less burdened by competition with groupmates. However, more research on bonobos in habitats with seasonal variation in food is needed. This study measured food availability and bonobo social organization at Luzaka, a new site in a seasonal forest fragment. Fruit abundance and dispersion were recorded for a year at Luzaka with the same methods used at Wamba, a bonobo site in more seasonally stable habitat and terrestrial herbaceous vegetation density was measured. At Luzaka, bonobo parties were also recorded for a year using camera traps. Fruit was more seasonal and dispersed at Luzaka than at Wamba. However, the social organization of Luzaka bonobos resembled social organization of bonobos at less seasonal sites. There were minor effects of fruit clumping on party size without effects on the proportion of females in parties suggesting that at Luzaka, the clumping of fruit slightly affected social cohesiveness but does not disproportionately affect females. Bonobo social cohesiveness and female gregariousness appears consistent and compatible with seasonal habitat.

Adaptive Party Choice of Low-Ranking Males in Fission-Fusion Dynamics of Chimpanzees in Kalinzu Forest Reserve, Uganda.

Several studies have examined factors that regulate fission-fusion dynamics (FFD) in chimpanzee communities, such as receptive females, predation risks, and food availability. However, the effects of these factors vary between populations. In this study, we conducted focal animal observations of adult males in the M group in Kalinzu to examine the influence of male dominance rank, aggression from other males, the presence of females exhibiting maximum sexual swelling (MS), and fruit abundance on male tendencies of party attendance. We found that low-ranking males spent more time alone than other males when females with MS were absent. In contrast, when females with MS were present, males of all ranks showed a similar tendency of party attendance. We also found that the aggressive interactions increased with the number of males irrespective of the presence or absence of females with MS, and low-ranking males attracted aggression more frequently than higher-ranking males. These results suggest that low-ranking males frequently ranged alone to avoid aggression from other males unless they attended parties to seek mating opportunities. We conclude that low-ranking males have alternative tactics to balance the costs and benefits incurred or gained when attending parties.

Why bonobos show a high reproductive skew towards high-ranking males: analyses for association and mating patterns concerning female sexual states.

Among non-human primates, male dominance rank is not necessarily a good indicator of mating success, and relationships between male dominance rank and mating or reproductive success are affected by female behavior and sexual states implying their probability of conception. Although comparisons of the behavior of male chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) suggest that the effect of male dominance rank on mating success is expected to be less prominent in bonobos, recent genetic studies have shown that high-ranking male reproductive skew is higher in bonobos than in chimpanzees. One possible reason for the higher reproductive skew in bonobos could be that female behavior and their sexual states may have much more influence on male mating and reproductive success in bonobos than in chimpanzees. In the current study on bonobos, we conducted focal animal observation of females and analyzed the influence of female sexual swelling, the number of days after parturition, and dominance rank of males on female associations, and copulation with adult males. Our results showed that females with maximum swelling (MS) had more proximity with high-ranking males and copulated more frequently with higher-ranking males than with lower-ranking males. Females for whom longer time had elapsed since parturition, and therefore had higher probabilities of conception, had 5-m proximity with adult males more frequently than females whom shorter time had elapsed since parturition, but did not have more copulation with adult males. Females with MS had proximity and copulated with high-ranking males frequently, which partly explains why the reproductive skew is so high in bonobos. These results are discussed in relation to previous hypotheses on the influence of long-lasting mother-son relationships on mating success of males and on the contribution of female receptivity during non-conceptive nursing periods to moderate intermale aggression in bonobos.

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.

Do female bonobos (Pan paniscus) disperse at the onset of puberty? Hormonal and behavioral changes related to their dispersal timing.

Natal dispersal is a milestone in an animal's life history, but its timing in developmental trajectories may differ between species. Although the two Pan species exhibit a similar pattern of female-biased dispersal, female bonobos (P. paniscus) leave their natal groups at an earlier age than female chimpanzees (P. troglodytes). As a preliminary step to explore the dispersal strategies of female bonobos, this study aimed to determine the relations of sexual swelling development, behavioral and hormonal activation, and first ovulation relative to dispersal timing. We measured levels of urinary estrone conjugates (E1C) and pregnanediol glucuronide (PdG) from 14 nulliparous females in wild bonobo groups at Wamba in the Democratic Republic of the Congo, and recorded their copulations with mature males. When close to dispersal, female bonobos exhibited swelling of the sexual skin (labia minora and perianal region) that did not reach the mature stage. Urinary E1C levels and copulation rates increased slightly before dispersal and greatly increased after dispersal. Ovulatory or gestatory signs implied by daily hormone profiles were not detected until one to two years after dispersal. Our findings indicate that female bonobos disperse at an early pubertal stage before ovulatory cycling is established. This earlier dispersal than sexual maturation could allow female bonobos to postpone reproduction-related energy costs until they become familiar with their new group or gain more time finding the group more suitable for successful reproduction in the future before actually settling. Further demographic and genetic data from dispersal to reproduction will help clarify their dispersal strategies.

Do immigrant female bonobos prefer older resident females as important partners when integrating into a new group?

Intergroup transfer is a critical part of the life history of group-living species, with considerable variation in its timings and patterns among species. Immigrant female bonobos are documented to smoothly integrate into a new group through forming affiliative relationships with old, high-ranking resident females (Idani, Folia Primatol 57:83-95, 1991). However, only a few studies are available on immigration costs and strategies for female bonobos. Here, we compared social relationships of natal females (known to be 4.5-7.2 years old) and immigrant females (estimated to be 6.8-12.3 years old) from one bonobo group at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo. Similar to previous studies, resident females did not appear to spatially isolate immigrant females or act aggressively toward them. However, resident males were more frequently aggressive toward immigrant females than toward natal females. Both natal and immigrant females tended to groom high-ranking females more than middle- and low-ranking females, although immigrant females spent more time grooming unrelated females than natal females. Immigrant females did not exhibit rank-related partner preference for genito-genital rubbing and copulation. Although we did not control for age differences because of the small sample size, our results provide partial support for the hypothesis that old female bonobos are important partners for the successful integration of young females into an unfamiliar group. This strategy could explain why female bonobos disperse before reaching sexual maturity, which contrasts with the need for female chimpanzees to display sexual swellings and draw male interest as protection against aggression from resident females.

Physical, behavioral, and hormonal changes in the resumption of sexual receptivity during postpartum infertility in female bonobos at Wamba.

The operational sex ratio (OSR) is used as a predictor for the intensity of mating competition. While many factors affect the OSR, there tends to be a high male bias in primate species with long interbirth intervals and non-seasonal breeding, such as hominid apes. However, the OSR of bonobos (Pan paniscus) is lower than that of chimpanzees (Pan troglodytes), which is thought to reduce competitive and aggressive male behaviors. The low OSR of bonobos is considered to result from the early resumption of female sexual receptivity during postpartum infertility and the receptivity that they continue to show until the late stage of pregnancy. In this study, we aimed to examine the early resumption of sexual receptivity by providing quantitative data on the resumption of maximal swelling (MS) in sexual skin and copulation, and changes in urinary estrone conjugate (E1C) concentrations during postpartum infertility in wild bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo. An analysis of 9 years of data revealed that females showed the first MS at 225.4 ± 132.7 days after parturition and performed the first copulation at 186.8 ± 137.5 days after parturition, both of which were in the early stage of postpartum infertility. The proportion of days with MS and the frequency of copulation steadily increased subsequently; however, the rate of increase gradually slowed approximately 42-48 months after parturition. There was a significant correlation between the proportion of days with MS and the frequency of copulation in each period for each female. We confirmed that E1C concentrations were significantly higher during the MS phase than during the non-MS phase. Data collected over 15 months on the E1C concentration during MS showed that it increased linearly from the early stage of lactation to the next conception. These results suggest that, although female bonobos do not usually conceive until 49.7 months after parturition, they resume MS and receptivity at a low level of E1C concentration during an early stage of postpartum infertility. This study of female bonobo receptivity and sex hormone changes during the postpartum non-fertile period provides important insights for examining the evolution of low OSR, which has been considered to contribute to peaceful social relationships among bonobos.

Prevalence of antibodies against human respiratory viruses potentially involving anthropozoonoses in wild bonobos.

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.

Body Site and Body Orientation Preferences during Social Grooming: A Comparison between Wild and Captive Chimpanzees and Bonobos.

Grooming site preferences have been relatively well studied in monkey species in order to investigate the function of social grooming. They are not only influenced by the amount of ectoparasites, but also by different social variables such as the dominance rank between individuals or their levels of affiliation. However, studies on this topic mainly come from monkey species, with almost no report on great apes. This study aimed to explore whether body site and body orientation preferences during social grooming show species-specific differences (bonobos vs. chimpanzees) and environment-specific differences (captivity vs. wild). Results showed that bonobos groomed the head, the front and faced each other more often than chimpanzees, while chimpanzees groomed the back, anogenitals and more frequently in face-to-back positions. Moreover, captive individuals were found to groom facing one another more often than wild ones, whereas wild individuals groomed the back and in face-to-back positions more. While future studies should expand their scope to include more populations per condition, our preliminary 2 by 2 comparison study highlights the influence of (i) species-specific social differences such as social tolerance, social attention and facial communication, and (ii) socioenvironmental constraints such as risk of predation, spatial crowding and levels of hygiene, that might be the two important factors determining the grooming patterns in two Panspecies.

Age and sex differences in juvenile bonobos in party associations with their mothers at Wamba.

Mothers are the most fundamental individuals for the survival and development of their immature offspring. Sex-biased dispersal has an effect on strong and long-lasting social bonding between mothers and their philopatric offspring. Nepotistic relationships are often seen in species with male-biased dispersal but less frequently in species with female-biased dispersal. Bonobos are unique among female-biased dispersal primates in that the females are codominant with males, exert influence on the mating opportunities of their mature sons, and tolerate each other regardless of relatedness. Few studies on bonobos have examined sex differences in social relationships between juveniles and their mothers, and how this relates to mother-son and female-female cooperative relationships amongst adults. We investigated whether the association index of juveniles with their mothers changed with age depending on the sex of the juveniles in parties of bonobos at Wamba, the Democratic Republic of the Congo. We found that female bonobos had decreased party associations with their mothers prior to their emigration from the natal group, while male bonobos maintained relatively high party associations with their mothers. These results indicate that sex differences that emerge during the juvenile period in bonobos in their spatial relationships with their mothers differ from previous findings on chimpanzees, spider monkeys, and muriquis, in which philopatric sons tend to spend less time in proximity to their mothers and disperse earlier than, or at a similar age to, daughters. The contrasts between bonobos and other primate species suggest that the high social status of female bonobos relative to that of males may facilitate the extension of maternal support for their philopatric sons, and that high tolerance among unrelated females may enable the spatial independence of daughters from their mothers at an earlier stage.

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, 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.

Comparisons of between-group differentiation in male kinship between bonobos and chimpanzees.

Patterns of kinship among individuals in different groups have been rarely examined in animals. Two closest living relatives of humans, bonobos and chimpanzees share many characteristics of social systems including male philopatry, whereas one major difference between the two species is the nature of intergroup relationship. Intergroup relationship is basically antagonistic and males sometimes kill individuals of other groups in chimpanzees, whereas it is much more moderate in bonobos and copulations between individuals of different groups are often observed during intergroup encounters. Such behavioural differences may facilitate more frequent between-group male gene flow and greater between-group differentiation in male kinship in bonobos than in chimpanzees. Here we compared differences between average relatedness among males within groups and that among males of neighbouring groups, and between-group male genetic distance between bonobos and chimpanzees. Contrary to expectation, the differences between average relatedness among males within groups and that among males of neighbouring groups were significantly greater in bonobos than in chimpanzees. There were no significant differences in autosomal and Y-chromosomal between-group male genetic distance between the two species. Our results showed that intergroup male kinship is similarly or more differentiated in bonobos than in chimpanzees.

Social influences on grooming site preferences in wild bonobos (Pan paniscus) at Wamba, DRC.

Social grooming is assumed to have both social and hygienic functions. In monkey species, body site preferences during social grooming are related to both the dominance ranks of participating individuals and strength of social bonds. It is suggested that low-ranking groomees and individuals with weak social bonds expose less vulnerable sites of their body because doing so allows them to avoid eye contact, thus reducing the risk of aggression. This study aimed to investigate the influence of (1) the levels of affiliation (through analyses of sex, grooming frequency, and group membership during intergroup encounters), (2) dominance, (3) kinship, and (4) age on grooming site preferences (head, front, back, anogenital region, and limbs) in wild bonobos. Subjects were two groups of wild bonobos living in Wamba, DR Congo. Body site preferences were documented from video clips. Our results illustrate that the levels of affiliation between individuals and their dominance status do not seem to influence body site preferences, contrasting with results in monkey species. However, the selection of body sites was mostly influenced by age and kinship. Mothers were found to groom less accessible sites on their immature offspring's body more than when grooming a non-related immature, suggesting that mothers invest in their offspring more to prevent diseases linked to ectoparasites. Finally, mature individuals groomed the inaccessible back more often than immature individuals, while the latter focused their grooming on the head and front. Overall, this study suggests hygienic functions of social grooming in wild bonobos.

Inter-group aggressive interaction patterns indicate male mate defense and female cooperation across bonobo groups at Wamba, Democratic Republic of the Congo.

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.

Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees.

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.

Bonobos' saliva remaining on the pith of terrestrial herbaceous vegetation can serve as non-invasive wild genetic resources.

Evaluating the genetic diversity of natural populations of endangered species is important for conservation. Although the genetic analysis of wildlife usually requires collecting DNA non-invasively, the variety of non-invasive DNA sampling methods is limited for each species. We present a method to obtain DNA of an endangered species, the bonobo (Pan paniscus), in which the pith of the terrestrial herbaceous vegetation (THV) that they consumed was newly utilized. We investigated the (1) frequency of encountering remnant saliva on three types of THV pith; (2) concentrations of DNA in the saliva samples by the real-time quantitative PCR; and (3) rates of positive PCR, accurate genotyping, and allelic drop out by analyzing two autosomal microsatellite loci (D7s817 and D9s910). The number of remnant saliva samples was recorded by following the bonobo groups on a daily basis. The frequency of encountering DNA samples was higher in saliva samples than in fecal samples. More than half of the saliva samples remaining on two types of THV pith provided sufficient concentrations of bonobo DNA (> 200 pg/µl). Rates of positive PCR and accurate genotyping were high, and allelic drop out rate was low when the amount of template DNA was above 200 pg per reaction. Our results suggest that the remnants of bonobo saliva on the pith of THV are a potential resource for obtaining DNA, and better than other kinds of samples from the perspective of the abundant sampling opportunities.

Bonobo and chimpanzee gestures overlap extensively in meaning.

Cross-species comparison of great ape gesturing has so far been limited to the physical form of gestures in the repertoire, without questioning whether gestures share the same meanings. Researchers have recently catalogued the meanings of chimpanzee gestures, but little is known about the gesture meanings of our other closest living relative, the bonobo. The bonobo gestural repertoire overlaps by approximately 90% with that of the chimpanzee, but such overlap might not extend to meanings. Here, we first determine the meanings of bonobo gestures by analysing the outcomes of gesturing that apparently satisfy the signaller. Around half of bonobo gestures have a single meaning, while half are more ambiguous. Moreover, all but 1 gesture type have distinct meanings, achieving a different distribution of intended meanings to the average distribution for all gesture types. We then employ a randomisation procedure in a novel way to test the likelihood that the observed between-species overlap in the assignment of meanings to gestures would arise by chance under a set of different constraints. We compare a matrix of the meanings of bonobo gestures with a matrix for those of chimpanzees against 10,000 randomised iterations of matrices constrained to the original data at 4 different levels. We find that the similarity between the 2 species is much greater than would be expected by chance. Bonobos and chimpanzees share not only the physical form of the gestures but also many gesture meanings.