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.     

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Male-male Interactions in Heterosexual and All-male Wild Mountain Gorilla Groups

Variation in male dispersal and behavior patterns are components of intraspecific differences in social systems. A comparison of male behavior in different social settings can be useful for determining which behavioral mechanisms contribute to variability in social systems. Two heterosexual multimale groups and one all-male group of mountain gorillas (Gorilla gorilla beringei) were observed for over 1100 h at the Karisoke Research Centre, Rwanda. Data on proximity patterns, dominance relationships, aggression, agonistic interventions, affiliation, and homosexual behavior were compared among the males in these groups to examine the influence of female presence, sex ratio, group size, and kinship on male—male interactions. Males in the all-male group stayed closer together, affiliated more, exhibited more homosexual behavior, and were more aggressive toward each other than males in heterosexual groups. However, the males in heterosexual groups showed more wounding and more consistent dominance relationships. Kinship did not influence male-male relationships in the all-male group. The males in the heterosexual groups rarely interacted with one another; they may actively avoid close proximity to reduce aggression. Results suggest that the variable social system of mountain gorillas may be more strongly influenced by demographic factors, male-female social relationships, and male-male competition for mates than by any benefits of male-male relationships.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Male chimpanzee behavior in relation to female ano-genital swelling

This study examined the relationships between male agonistic, affiliative, and sexual behaviors and female estrus condition in captive adolescent and young-adult chimpanzees (Pan troglodytes). Data on agonistic, affiliative, and sexual behaviors of 11 males living in three social groups were collected during daily 45 minute observations over a 5 month period. Female estrus condition was assessed daily using the relative size of the female's ano-genital swelling. It was hypothesized that the presence of maximally tumescent females would generate conflicts between males, so an increase in inter-male agonism was predicted. Males exhibited higher rates of agonism toward other males when at least one female in the group was maximally tumescent. Male affiliative behavior directed toward other males and social play with males were affected by the presence and number of maximally tumescent females. Male sexual behavior increased when maximally tumescent females were present.     

Grooming interactions among adult chimpanzees at Bossou,Guinea, with special reference to social structure

Grooming and proximity interactions among chimpanzees at Bossou, Republic of Guinea, were analyzed as an index of friendly and affinitive relationships among adult males, among adult females, and between the sexes. Data from the first (1976–1977) and the third (1982–1983) study period were used. The expected value of their interactions was calculated from the number of adult males and females in the group and also from the observed frequency of combinations of adult males and females in the parties (temporary foraging groups). In the pooled data from the two periods, there was little difference between grooming and proximity (without grooming). The frequency of male-female grooming and proximity interactions was lower than expected, and that of female-female interactions was higher than expected. The frequencies of male-male grooming and proximity were intermediate but fluctuated. Male-male grooming frequency was lower than that recorded in chimpanzees of East Africa. Characteristics of same-sex affinitive interactions, especially between Bossou chimpanzee females, clearly differ from those of East African chimpanzees and are more like those recorded for female-related groups of Japanese macaques (Macaca fuscata).These differences indicate the variability and flexibility of chimpanzee social structure.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.     

Female life history and mating patterns among the M group chimpanzees of the Mahale national park,Tanzania

The mating behavior of receptive females in the M group chimpanzees (Pan troglodytes schweinfurthii) of the Mahale Mountains, western Tanzania, was studied by intensive sampling over a period of 5 months. Restrictive matings were observed only between parous females mostly in the ovulatory stage and prime adult males, in particular the alpha. Young, nulliparous and/or non-ovulatory females tended to mate with immature or low-ranking adult males. By contrast, older, parous and/or ovulatory females tended to mate with adult and higher-ranking males. These confirmed the results of a previous extensive study of the same group. In addition, gradual shift from opportunistic to restrictive matings after inter-unit-group transfer was revealed for 2 ex-K-group parous females. The findings were discussed in relation to the life history of female chimpanzees. A National Park since 1984.     

Social interactions and aggression among male Madagascar hissing cockroaches (Gromphadorhina portentosa) in groups (Dictyoptera: Blaberidae)

We studied agonistic interactions among male Madagascar hissing cockroaches,Gromphadorhina portentosa, in groups of five (low-density) or 10 (high-density) males. Consistent with previous studies of male pairs, we observed aggression (Abdomen Flick, Abdomen Push, Butt, Lunge), submission (Crouch, Retreat), and noncontact behavior (Abdominal Extension, Abdomen Thrash, Agonistic Hiss, Stilt). Males at both densities performed all acts. However, males in the high-density group performed Abdomen Push significantly more often than males at a low density. The rate of each remaining act was unaffected by density. Regardless of density, males within social groups varied in aggression. More aggressive males utilized frontal assaults (Butt and Lunge) during interactions, while males displaying lower levels of aggression preferentially used the abdomen during interactions. More aggressive males performed Abdomen Flick more frequently, while males displaying lower levels of aggression performed Abdomen Push. We also investigated the relationship between male aggression and the four noncontact behaviors. We found that Abdominal Extension, Abdomen Thrash, and Agonistic Hiss were positively correlated with our aggregate measure of male aggression suggesting these are aggressive displays. Stilt was positively correlated with measures of both aggression and submission, leaving its function unclear. None of the behavioral acts examined in this study were highly correlated with male weight. Our results are discussed in light of possible hypotheses addressing the function of specific behavior during male-male competition.     

Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a preliminary study

The dichotomy between the two Pan species, the bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) has been strongly emphasized until very recently. Given that most studies were primarily based on adult individuals, we shifted the “continuity versus discontinuity” discussion to the infant and juvenile stage. Our aim was to test quantitatively, some conflicting statements made in literature considering species differences between immature bonobos and chimpanzees. On one hand it is suggested that infant bonobos show retardation in motor and social development when compared with chimpanzees. Additionally it is expected that the weaning process is more traumatic to chimpanzee than bonobo infants. But on the other hand the development of behaviors is expected to be very similar in both species. We observed eight mother–infant pairs of each species in several European zoos. Our preliminary research partially confirms that immature chimpanzees seem spatially more independent, spending more time at a larger distance from their mother than immature bonobos. However, the other data do not seem to support the hypothesis that bonobo infants show retardation of motor or social development. The development of solitary play, environmental exploration, social play, non-copulatory mounts and aggressive interactions do not differ between the species. Bonobo infants in general even groom other group members more than chimpanzee infants. We also found that older bonobo infants have more nipple contact than same aged chimpanzees and that the weaning process seems to end later for bonobos than for immature chimpanzee. Additionally, although immature bonobos show in general more signs of distress, our data suggest that the weaning period itself is more traumatic for chimpanzees.     

Postconflict Affiliation Between Former Opponents in Macaca thibetana on Mt. Huangshan, China

We describe basic patterns of postconflict affiliation between former opponents within a group of wild, provisioned Tibetan macaques Macaca thibetana on Mt. Huangshan, China. Like most primates studied to date, Tibetan macaques reconciled, i.e., overall they engaged in affiliative interaction with opponents at higher rates immediately after an aggressive conflict than at other times. Probabilities of affiliation were enhanced ≤30 s after the end of hostilities. However when we examined sex partner combinations separately, we found unequivocal evidence for reconciliation only for male-male dyads. Tolerant interaction among other partner combinations apparently was not disrupted after a conflict, presumably obviating the need to reconcile. One aspect of reconciliation among males was consistent with other indications of a despotic dominance style: aggressors initiated a higher proportion of affiliative interactions after a conflict than at other times. Another aspect of reconciliation was more typical of relaxed dominance styles: males used specialized behaviors (embraces and same-sex mounts) disproportionately to reconcile. We also found inconsistent evidence for the valuable relationship hypothesis; probabilities of reconciliation were enhanced for male-male dyads with the closest affiliative relationships, but not for those that displayed the most tolerance or mutual agonistic support. We discuss reconciliation and other aspects of conflict management among males in the context of a group with nearly even sex ratios and high male-male mating competition.     

Social Relationships among Males in Multimale Siamang Groups

I quantified social and spatial interactions among adults in 4 multimale siamang (Symphalangus syndactylus) groups to evaluate the importance of aggression and avoidance in mediating male-male relationships. Actual genetic relationships among adults are unknown, but available mitochondrial data suggest that in 3 of 4 groups, neither male was the offspring or maternal sibling of the female, whereas in the fourth group, a matrilineal relationship between the female and 1 adult male was not excluded. Rates of aggression involving male-male dyads were very low. One male-female dyad maintained closer spatial cohesion than those of other adult dyads in 3 of 4 groups. Nonetheless, all adult males spent substantial percentages of their time ≤20 m from other adults in their groups. The percentages of time that male-male dyads spent in social grooming interactions did not differ from those of male-female dyads. In 3 groups, both males copulated with the group female. While previous studies have reported high rates of aggression between adult males and subadult male group members in siamangs, my results suggest that male-male relationships in multimale groups at Way Canguk were relatively harmonious. Acceptance of multimale grouping (and in some cases sexual polyandry) suggests that the benefits outweigh the costs under some circumstances. If there was a genetic relationship between males, then tolerance of delayed dispersal and copulation with the adult female may function as a form of parental investment. Males may also benefit from multimale grouping via enhanced territorial defense or reduced costs of mate defense.     

Factors underlying party size differences between chimpanzees and bonobos: a review and hypotheses for future study

Differences in party size and cohesiveness among females have been primary topics in socio-ecological comparisons of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). This paper aims to review previous studies that attempted to explain these differences and propose some hypotheses to be tested in future studies. Comparisons of recent data show that relative party size (expressed as a percentage of total group size) is significantly larger for bonobos than chimpanzees. Although the prolonged estrus of females, close association between mother and adult sons, female social relationships including unique homosexual behavior, and high female social status might be related to the increased party size and female cohesiveness of bonobos, these social and behavioral factors alone do not appear to explain the differences between the two species. Differences in ecological factors, including fruit-patch size, density of terrestrial herbs, and the availability of scattered foods that animals forage as they travel between large fruit patches could also contribute to the differences between chimpanzees and bonobos. However, these factors cannot fully account for the increased party size and female cohesiveness of bonobos. The higher female cohesiveness in bonobos may be explained by socio-ecological systems that reduce the cost in feeding efficiency incurred by attending mixed-sex parties. These systems may include female initiatives for party ranging movements as well as the factors mentioned above. Because of their geographical isolation, the two species probably evolved different social systems. Chimpanzees, whose habitats became very dry during some periods in the Pleistocene, likely evolved more flexible fission–fusion social systems to cope with seasonal and annual variation in food availability. On the other hand, bonobos had a large refugia forest in the middle of their range even during the driest periods in the Pleistocene. Therefore bonobos, whose habitats had more abundant food and smaller variation in food availability, probably evolved systems that help females stay in mixed parties without incurring large costs from contest and scramble competition.     

Group unity of chimpanzees elucidated by comparison of sex differences in short-range interactions in Mahale Mountains National Park,Tanzania

Chimpanzees (Pan troglodytes) form multi-male and multi-female unit groups with fission–fusion grouping patterns. Short-range interaction (SRI) plays an important role in the unity of these groups and in maintaining social bonds among members. This study evaluated three models of chimpanzee social structure that differed according to the emphasis each placed on social bonds between the sexes, i.e., the male-only, the bisexual, and the male-bonded unit-group model. I investigated differences in SRI between the sexes among group members in well-habituated wild chimpanzees in Mahale Mountains National Park, Tanzania. I followed six focal adult males and six females, and quantified their respective SRI with other chimpanzees. Except between subordinate males and adult females, adults in general engaged in SRI with about 60–90% of the individuals with whom they made visual contact each day, whether in large or small parties. Although the number of social grooming (SGR) partners was limited, male–male SGR networks were wider than were either male–female or female–female SGR networks among adults. The number of contact-seeking behavior (CSB) partners was also limited, but dominant males had more CSB partners. Adult females mainly interacted by pant-grunt greeting (PGG) with adult males, but tended to do so mainly with the highest-ranking male(s) within visual contact. These results indicated that the social bonds among adult males were essential to group unity. Because of clear male dominance, adult females established peaceful coexistence with all group members despite less frequent SRI with subordinate males by maintaining affiliative social bonds with dominant males, thereby supporting the male-bonded unit-group model. Adult females had many female SRI partners, but these interactions did not involve performing conspicuous behaviors, suggesting that females maintain social bonds with other females in ways that differ from how such bonds are maintained with and between adult males.     

Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships

This study compares adult play behavior in the two Pan species in order to test the effects of phylogenetic closeness and the nature of social systems on play distribution. The social play (both with fertile and immature subjects) performed by adults did not differ between the two species. In contrast, in bonobos, play levels among fertile subjects were higher than in chimpanzees. Findings regarding levels of undecided conflicts (more frequent in bonobos) and formal submission displays (lacking in bonobos) confirm, in the two colonies under study, that bonobos exhibit "egalitarianism" more than chimpanzees. Some authors emphasized the importance of play-fighting for social assessment when relationships among individuals are not codified and structured according to rank-rules. Indeed, adult bonobos played more roughly than chimpanzees. Moreover, adult bonobos displayed the full play-face at a high frequency especially during rough play sessions, whereas in chimpanzees, the frequency of play signals was not affected by roughness of play. The frequency of social play among bonobo females was higher than in any other sex combinations, whereas no difference was found for chimpanzees. As a matter of fact, social play can be viewed as a balance between cooperation and competition. Among bonobo females, characterized by social competence and affiliation, social play might enhance their behavioral flexibility and increase their socially symmetrical relationships which, after all, are the basis for their egalitarian society.     

Sex differences in copulation attempts in wild bonobos at Wamba

We examined sex differences in copulation attempts in a group of wild bonobos at Wamba, Congo, by analyzing the behavioral sequence. Most copulation attempts were initiated by approach or courtship behaviors by males. Males showed these behaviors when they were more than 5 m from females, whereas females did so only when males solicited them from within 5 m. Most copulations involved females showing perineal swelling, because males solicited those females more frequently and those females accepted copulation more frequently than did females in the non-swelling phase. Nevertheless, males solicited females in the non-swelling phase in one-third of copulation attempts, and those females accepted copulation in half of those attempts. This is markedly different from chimpanzees, in which sexual behaviors almost exclusively involve females in the swelling phase. The perineum of female bonobos during the non-swelling phase is soft and wrinkled but fairly large, which may attract males to some extent. The low, but existing, attractiveness and receptivity of female bonobos during the non-swelling phase might have evolved to control sexual competition among males and provide higher social status for females.     

Female Coalitions Against Male Aggression in Wild Chimpanzees of the Budongo Forest

In the wild, female chimpanzees (Pan troglodytes) are subject to male aggression that at times can be prolonged or particularly violent. There are no reports of cooperative retaliation to such aggression, a strategy observed in the congeneric Pan paniscus, from the wild despite >4 decades of detailed behavioral study across a number of populations and its occurrence among captive female chimpanzees. If the reports from captivity represent an inherent capacity, then the absence of similar reports from wild populations suggests that females may be able to form coalitions only under appropriate ecological and demographic conditions. During a study of male and female aggressive interactions among chimpanzees of the Budongo Forest, Uganda, wild adult female chimpanzees sometimes formed coalitions with one another to retaliate against male aggression. This may be possible because these females tend to be more gregarious than in other populations of East African chimpanzees, as other studies of the same population have suggested; the extent and variation of female chimpanzee social strategies may, therefore, need reconsideration. Further, my observations strengthen the argument that at least some of the differences between chimpanzees and bonobos may be more of degree than of kind.     

Male-mediated gene flow in patrilocal primates

Background

Many group–living species display strong sex biases in dispersal tendencies. However, gene flow mediated by apparently philopatric sex may still occur and potentially alters population structure. In our closest living evolutionary relatives, dispersal of adult males seems to be precluded by high levels of territoriality between males of different groups in chimpanzees, and has only been observed once in bonobos. Still, male–mediated gene flow might occur through rare events such as extra–group matings leading to extra–group paternity (EGP) and female secondary dispersal with offspring, but the extent of this gene flow has not yet been assessed.

Methodology/Principal Findings

Using autosomal microsatellite genotyping of samples from multiple groups of wild western chimpanzees (Pan troglodytes verus) and bonobos (Pan paniscus), we found low genetic differentiation among groups for both males and females. Characterization of Y–chromosome microsatellites revealed levels of genetic differentiation between groups in bonobos almost as high as those reported previously in eastern chimpanzees, but lower levels of differentiation in western chimpanzees. By using simulations to evaluate the patterns of Y–chromosomal variation expected under realistic assumptions of group size, mutation rate and reproductive skew, we demonstrate that the observed presence of multiple and highly divergent Y–haplotypes within western chimpanzee and bonobo groups is best explained by successful male–mediated gene flow.

Conclusions/Significance

The similarity of inferred rates of male–mediated gene flow and published rates of EGP in western chimpanzees suggests this is the most likely mechanism of male–mediated gene flow in this subspecies. In bonobos more data are needed to refine the estimated rate of gene flow. Our findings suggest that dispersal patterns in these closely related species, and particularly for the chimpanzee subspecies, are more variable than previously appreciated. This is consistent with growing recognition of extensive behavioral variation in chimpanzees and bonobos.