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.

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.

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.

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.

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.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts.

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

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.

The gestural repertoire of the wild bonobo (Pan paniscus): a mutually understood communication system.

In animal communication, signallers and recipients are typically different: each signal is given by one subset of individuals (members of the same age, sex, or social rank) and directed towards another. However, there is scope for signaller-recipient interchangeability in systems where most signals are potentially relevant to all age-sex groups, such as great ape gestural communication. In this study of wild bonobos (Pan paniscus), we aimed to discover whether their gestural communication is indeed a mutually understood communicative repertoire, in which all individuals can act as both signallers and recipients. While past studies have only examined the expressed repertoire, the set of gesture types that a signaller deploys, we also examined the understood repertoire, the set of gestures to which a recipient reacts in a way that satisfies the signaller. We found that most of the gestural repertoire was both expressed and understood by all age and sex groups, with few exceptions, suggesting that during their lifetimes all individuals may use and understand all gesture types. Indeed, as the number of overall gesture instances increased, so did the proportion of individuals estimated to both express and understand a gesture type. We compared the community repertoire of bonobos to that of chimpanzees, finding an 88 % overlap. Observed differences are consistent with sampling effects generated by the species' different social systems, and it is thus possible that the repertoire of gesture types available to Pan is determined biologically.

Personality in wild bonobos (Pan paniscus).

To understand the evolution of personality structure requires examining personality dimensions in multiple species using a common set of traits. Little research has been conducted on personality in wild populations of nonhuman primates. Using behavioral observations and questionnaire ratings, we examined factors influencing personality in 16 wild bonobos (Pan paniscus) at Wamba, Luo Scientific Reserve, Democratic Republic of the Congo. We extracted five factors from 31 of the items from the Hominoid Personality Questionnaire (HPQ) and three factors from observed behaviors. The HPQ factors were labeled UnemotionalityQ , FriendlinessQ , AggressivenessQ , IrritabilityQ , and ActivityQ . The behavioral factors were labeled GroomingB , PlayfulnessB , and IntroversionB . We established the convergent and divergent validity of these factors by obtaining correlations between the HPQ and behavioral factors. We tested for sex differences and found that males were significantly higher on IntroversionB and significantly lower in IrritabilityQ . We then tested for age differences and found that FriendlinessQ was lower and AggressivenessQ was higher in older individuals. Finally, we found that, among males, hierarchical rank was associated with higher AggressivenessQ . These findings contrast with findings in chimpanzees in ways consistent with known species differences. For one, consistent with the more egalitarian structure of bonobo society, we did not identify a clear Dominance factor. Also, the results related to sex differences were consistent with previous findings that reveal closer bonds between female bonobos than female chimpanzees. These findings highlight the importance of studying personality in closely related species and the need to consider species' socioecology when studying personality. Am. J. Primatol. 78:1178-1189, 2016. © 2016 Wiley Periodicals, Inc.

How did bonobos come to range south of the congo river? Reconsideration of the divergence of Pan paniscus from other Pan populations.

While investigating the genetic structure in wild bonobos,(1) we realized that the widely accepted scenario positing that the Pleistocene appearance of the Congo River separated the common ancestor of chimpanzees (Pan troglodytes) and bonobos (P. paniscus) into two species is not supported by recent geographical knowledge about the formation of the Congo River. We explored the origin of bonobos using a broader biogeographical perspective by examining local faunas in the central African region. The submarine Congo River sediments and paleotopography of central Africa show that the Congo River has functioned as a geographical barrier for the last 34 million years. This evidence allows us to hypothesize that when the river was first formed, the ancestor of bonobos did not inhabit the current range of the species on the left bank of the Congo River but that, during rare times when the Congo River discharge decreased during the Pleistocene, one or more founder populations of ancestral Pan paniscus crossed the river to its left bank. The proposed scenario for formation of the Congo River and the corridor hypothesis for an ancestral bonobo population is key to understanding the distribution of great apes and their evolution.

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 group's 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.

Examining infantile facial features and their influence on caretaking behaviors in free-ranging Japanese macaques (Macaca fuscata).

Facial features of immature individuals play a pivotal role in eliciting caretaking behaviors in humans. It has been posited that non-human animals share particular infantile facial features with humans, which can elicit caregivers' attention and caretaking behaviors. Nevertheless, the empirical examination of this hypothesis is extremely limited. In this study, we investigated infantile facial features in Japanese macaques (Macaca fuscata), their developmental processes, and their correlation with caretaking and infant behaviors, based on 470 facial photographs from one free-ranging group. We measured the size of facial parts and evaluated these features using non-contact procedures with the animals. The results indicated that, although some partial species differences were observed, the infantile facial features in Japanese macaques were broadly consistent with those previously observed in humans and great apes. Furthermore, half of the infant subjects displayed non-linear developmental trajectories of infantile faces, similar to those suggested in humans. However, unlike previous studies in humans, infantile faces were not significantly associated with maternal or non-maternal caretaking behaviors, nor were their developmental changes correlated with infant behavioral development. These findings indicate that while many aspects of infantile facial features are shared among particular primates, humans may have evolved a uniquely elevated preference for selecting such features among the primate lineage.

Comparative analysis of intragroup intermale relationships: a study of wild bonobos (Pan paniscus) in Wamba, Democratic Republic of Congo and chimpanzees (Pan troglodytes) in Kalinzu Forest Reserve, Uganda.

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) share a multi-male/multi-female societal organization and form male-philopatric groups, disparities in terms of male aggression and stability of temporary parties are thought to exist among them. However, existing research in bonobos has mainly focused on the high social status, prolonged receptivity, and characteristic sexual behaviors of females, leaving the behaviors of males understudied. Moreover, prior comparative studies on Pan suffer from methodological inconsistencies. This study addresses these gaps by employing a uniform observation method to explore party attendance and aggressive interactions among male bonobos in Wamba and male chimpanzees in Kalinzu. Unlike male chimpanzees, which exhibit dispersion in the absence of receptive females in the group, male bonobos showed a lesser degree of such dispersion. Although the overall frequency of aggressive interactions per observation unit did not significantly differ between the two species, the nature of these interactions varied. Notably, severe aggressive behaviors such as physical confrontations among adult males were absent in bonobos, with most aggression occurring between the sons of the two highest-ranking females. Additionally, in bonobos, females actively engaged in polyadic aggressive behavior as aggressors, while all instances of coalitionary aggression in chimpanzees originated from male aggressors. These findings underscore the substantial impact of female behaviors on the observed distinctions in male aggressive interactions between the two species.

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.

Molecular diversity of entodiniomorphid ciliate Troglodytella abrassarti and its coevolution with chimpanzees.

The entodiniomorphid ciliate Troglodytella abrassarti is a colonic mutualist of great apes. Its host specificity makes it a suitable model for studies of primate evolution. We explored molecular diversity of T. abrassarti with regard to large geographical distribution and taxonomic diversity of its most common host, the chimpanzee. We found a very low diversification of T. abrassarti in chimpanzees across Africa. Distribution of two types of T. abrassarti supports evolutionary separation of the Western chimpanzee, P. t. verus, from populations in Central and East Africa. Type I T. abrassarti is probably a derived form, which corresponds with the Central African origin of chimpanzees and a founder event leading to P. t. verus. Exclusivity of the respective types of T. abrassarti to Western and Central/Eastern chimpanzees corroborates the difference found between an introduced population of presumed Western chimpanzees on Rubondo Island and an autochthonous population in mainland Tanzania. The identity of T. abrassarti from Nigerian P. t. ellioti and Central African chimpanzees suggests their close evolutionary relationship. Although this contrasts with published mtDNA data, it corroborates current opinion on the exclusive position of P. t. verus within the chimpanzee phylogeny. The type of T. abrassarti occurring in Central and East African common chimpanzee was confirmed also in bonobos. This may point to the presence of an ancestral Type II found throughout the Lower Guinean rainforest dating back to the common Pan ancestor. Alternatively, the molecular uniformity of T. abrassarti may imply a historical overlap of the species' distribution ranges.

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.

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.

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.

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.

Female contributions to the peaceful nature of bonobo society.

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are closely related, females of the two species show surprisingly large differences in many behavioral aspects. While female chimpanzees tend to range alone or in small parties during non-estrous periods, female bonobos aggregate even more often than do males. Female chimpanzees do not have frequent social interactions with other females, whereas female bonobos maintain close social associations with one another. Although the ranging patterns of chimpanzee parties are generally led by males, female bonobos often take the initiative in ranging behavior. While female chimpanzees usually do not exhibit estrus during postpartum amenorrhea or pregnancy, female bonobos exhibit a prolonged pseudo-estrus during such non-conceptive periods. Studies of these two species have also shown great differences in agonistic behaviors performed by males. Male chimpanzees frequently fight with other males to compete for estrous females, but male bonobos seldom do so. While there are many records of infanticide by male chimpanzees, there is no confirmed record of such an event among bonobos. Several cases of within-group killing among adult male chimpanzees have been reported, but there is no such record for bonobos. While intergroup conflicts among chimpanzees sometimes involve killing members of the other group, intergroup conflicts among bonobos are considerably more moderate. In some cases, bonobos from two different groups may even range together for several days while engaging in various peaceful interactions. I will address two important questions that arise from these comparisons, exploring why females of such closely related species show such clear differences in behavior and whether or not the behavioral characteristics of female bonobos contribute to the peaceful nature of bonobo society.